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The polyvagal perspective

Stephen W. Porges

University of Illinois at Chicago, Brain-Body Center, Department of Psychiatry (mc 912),

Chicago, IL 60612, United States

Accepted 26 June 2006

Available online 16 October 2006

Abstract

The polyvagal theory introduced a new perspective relating autonomic function to behavior, that included an appreciation of the autonomic

nervous system as a ‘‘system,’’ the identiﬁcation of neural circuits involved in the regulation of autonomic state, and an interpretation of autonomic

reactivity as adaptive within the context of the phylogeny of the vertebrate autonomic nervous system. The paper has two objectives: ﬁrst, to

provide an explicit statement of the theory; and second, to introduce the features of a polyvagal perspective. The polyvagal perspective emphasizes

how an understanding of neurophysiological mechanisms and phylogenetic shifts in neural regulation leads to different questions, paradigms,

explanations, and conclusions regarding autonomic function in biobehavioral processes than peripheral models. Foremost, the polyvagal

perspective emphasizes the importance of phylogenetic changes in the neural structures regulating the autonomic nervous system and how

these phylogenetic shifts provide insights into the adaptive function and the neural regulation of the two vagal systems.

Keywords: Autonomic nervous system; Heart rate variability; Respiratory sinus arrhythmia; Vagus; Polyvagal theory; Parasympathetic; Respiration; Vagal tone;

Evolution; Phylogeny

1. Overview

The polyvagal theory (Porges, 1995) introduced a new

perspective relating autonomic function to behavior. This

perspective includes an appreciation of the autonomic nervous

system as a ‘‘system,’’ the identiﬁcation of neural circuits

involved in the regulation of autonomic state, and an

interpretation of autonomic reactivity as adaptive within the

context of the phylogeny of the vertebrate autonomic nervous

system. The polyvagal theory encourages a level of inquiry that

challenges scientists to incorporate an integrative understanding

of the role neural mechanisms play in regulating biobehavioral

processes. The polyvagal theory requires an expansive con-

ceptualization of the autonomic nervous system to include target

organ afferent and efferent pathways, and a quest to understand

the reciprocal inﬂuences and bidirectional communication

between the heart and the central nervous system. The polyvagal

theory provides a ‘‘perspective’’ to frame research questions and

is not a static theory. Thus, as knowledge of neurophysiology

increases, testable hypotheses will shape and expand the theory.

The paper has two primary objectives: ﬁrst, to provide an

explicit statement of the theory; and second, to introduce the

features of a polyvagal perspective. The theory and perspective

are discussed within the context of the history of psychophy-

siology. The polyvagal theory provides an important bridge

from a correlative approach, that historically characterized

psychophysiology, to a more integrative model, incorporating

contemporary knowledge from neurophysiology and vertebrate

phylogeny. The polyvagal perspective emphasizes how an

understanding of neurophysiological mechanisms and phylo-

genetic shifts in neural regulation leads to different questions,

paradigms, explanations, and conclusions regarding autonomic

function in biobehavioral processes than peripheral models.

2. The polyvagal theory

2.1. Introduction

The ability to monitor, conceptualize, and interpret heart rate

variability (HRV) is dependent on technologies for observing the

beating of the heart, methodologies for quantifying heart rate

parameters, knowledge of underlying neural mechanisms

mediating beat-to-beat changes, and neurophysiological models

linking autonomic regulation to psychological, physiological,

www.elsevier.com/locate/biopsycho

Biological Psychology 74 (2007) 116–143

The preparation of this manuscript was supported, in part, by grants MH

067446 and MH 60625 from the National Institutes of Health.

E-mail address: sporges@uic.edu.

doi:10.1016/j.biopsycho.2006.06.009

and behavioral processes. Technologies and methodologies

metaphorically provide windows of observation into the assumed

neural mechanisms that can result in either clear or blurred

representations. However, models and theories, which organize

knowledge and generate plausible explanations, drive research

and create the need for speciﬁc methods. Without plausible

models to synthesize information from various disciplines, it

would be difﬁcult to test hypotheses that would link peripheral

autonomic function to neurophysiological theory or clinical

status.

Psychophysiology is at the crossroads of several disciplines,

each with preferred models, paradigms, and measures. Unlike

physiology, with its focus on mechanism and structure, or

cardiology, with its focus on clinical status, psychophysiology

historically was driven by paradigms derived from psychology,

often treating physiological parameters as if they were

observable behaviors. The early psychophysiologists, deﬁned

by their use of the polygraph, applied the polygraph to

‘‘transform’’ unobservable psychological or mental processes

into measurable physiological variables (e.g., Razran, 1961).

The early issues of Psychophysiology echo this strategy with

articles describing an aphysiological treatment of physiological

variables and a disinterest in neural mechanisms mediating the

variables measured. Although the measures of physiological

activity were operationally deﬁned and diligently quantiﬁed, the

parameters of the physiological processes measured were

selected independent of either knowledge of or interest in a

neurophysiological model encompassing the dynamic feedback

nature of the autonomic nervous system. Even today, few

psychophysiologists are trained in neuroanatomy or neurophy-

siology. In the early days of psychophysiology, physiological

variables, transformed into an observable tracing on the

polygraph, were treated similarly to overt behaviors or subjective

reports. Consistent with an emphasis of treating physiology, as if

it were a behavior, most psychophysiological studies applied S–

R paradigms in which the stimulus was a sensory variable or

psychological task, and the responsewas a physiological variable

(see Stern, 1964). In fact, an attempt was made to use these

paradigm constraints to deﬁne psychophysiology and to

distinguish psychophysiology from physiological psychology,

the latter being a discipline focused on manipulating physiology

and monitoring behavior. This strict deﬁnition of psychophy-

siology no longer characterizes current research, as psychophy-

siologists have embraced several paradigms and incorporated an

interest in the nervous system. However, an aphysiological

‘‘operational’’ model still dominates the literature and greatly

inﬂuences how HRV is quantiﬁed and interpreted in the literature.

For example, various strategies to quantify RSA have focused on

phenomenological features (e.g., relation to respiration) and not

on neurophysiological (e.g., medullary interneurons, neuropep-

tides, neurotransmitters) or neuroanatomical features (e.g.,

source nuclei of vagal efferent pathways).

2.2. History of HRV

Most studies investigating HRV have occurred during the

past 40 years. Clinical interpretations and applications have an

even shorter history. Integrative theories that link central

nervous system structures to autonomic function, such as the

polyvagal theory (Porges, 1995, 2003), have only emerged

during the past few years (Berntson et al., 1994; Benarroch,

1993; Craig, 2005; Critchley, 2005; Taylor et al., 1999; Thayer

and Lane, 2000). The study of HRV requires methods with a

sufﬁcient precision to accurately time beat-to-beat changes.

Since this methodology was inaccessible to many researchers,

the study of HRV had a slow trajectory within psychophysiol-

ogy. When HRV was initially presented as a variable at the

Society for Psychophysiological Research, several prominent

psychophysiologists (even former presidents of the society)

adamantly argued that HRV was an artifact due to poor

experimental control. From their perspective, the heart had a

stable rhythm and either decelerated or accelerated in response

to speciﬁc stimulus conditions. To demonstrate that HRV was

both an individual difference and a response variable, methods

needed to be developed to accurately measure beat-to-beat

changes. Techniques were developed to detect and to time

accurately the onset of sequential heart beats. Engineers

developed electrical circuits to identify the peak of R-waves

and to time the intervals between successive heart beats with

millisecond accuracy. With the advent of laboratory computers

and the availability of analog to digital converters, timing

became more precise and accurate and computer algorithms

were able to detect R-waves and other components of the ECG.

Prior to the accurate timing with laboratory computers, R–R

intervals were quantiﬁed by measuring the distance between R-

waves with a ruler or using a ruler to measure the output of the

cardiotachograph. The cardiotachograph, invented by Boas (see

Boas and Goldschmidt, 1932), was a welcomed addition to the

Grass and Offner (Beckman) polygraphs that populated and

deﬁned the psychophysiologist’s laboratory in the 1960s. The

cardiotachograph not only provided instant visual feedback of

heart rate changes, but also reduced the expense of polygraph

paper by enabling the paper speed to run slower without

inﬂuencing the accuracy of measurement.

Since measurement and quantitative procedures were far from

standardized, in early research there is little distinction between a

global concept of sinus arrhythmia and the more speciﬁc

rhythmicity of respiratory sinus arrhythmia (RSA). Research on

HRV initially progressed in two directions. First, there was a

dominant trend towards understanding the physiological

mechanisms mediating RSA. Second, clinical medicine identi-

ﬁed speciﬁc relationships between global measures of HRV and

clinical status. These two directions co-existed prior to the

emergence of psychophysiology. However, in the late 1960s,

with the availability of polygraphs in academic laboratories, a

third trend appeared as psychophysiologists began to system-

atically investigate the relationship between psychological

processes and HRV (e.g., Porges and Raskin, 1969).

2.3. Early studies related HRV to physiological

mechanisms

Although not exhaustive, several historical studies highlight

the emergence of HRV as a physiologically meaningful

S.W. Porges / Biological Psychology 74 (2007) 116–143 117

measure. References to RSA were made in the early 1900s.

Wundt (1902) stated that ‘‘... respiratory movements are

therefore regularly accompanied by ﬂuctuations of the pulse,

whose rapidity increases in inspiration and decreases in

expiration.’’ The functional relation between the amplitude of

RSA and the concept of vagal tone was clearly stated by Hering

(1910). Hering reported that breathing provided a functional

test of vagal control of the heart. Hering stated that ‘‘it is known

with breathing that a demonstrable lowering of heart rate ... is

indicative of the function of the vagi.’’ Bainbridge (1920)

attempted to explain RSA in terms of alterations in barore-

ceptor and volume receptor responses to changes in blood ﬂow

caused by changes in thoracic pressure associated with respi-

ration. Anrep et al. (1936) investigated the inﬂuence of several

physiological parameters on RSA, including: the inﬂuence of

respiratory rate and amplitude, blood gas concentrations, and

efferent cardioregulatory neural pathways.

2.4. Early studies using HRV as a clinical indicator

Eppinger and Hess (1915) stated that ‘‘... clinical facts,

such as respiratory arrhythmia, habitual bradycardia, ... have

furnished the means of drawing our attention to the variations in

the tonus of the vagal system in man.’’ Although Eppinger and

Hess were interested in clinical medicine, their case studies

described a relation between clinical problems in the regulation

of autonomic function that did not have, with the available

technology, a morphological correlate. Their observations are

relevant to contemporary psychophysiological investigation of

HRV for several reasons, including: (1) they alerted us to the

importance of the vagus in mediating atypical physiological

responses; (2) they related individual differences in vagal

inﬂuences to individual differences in psychiatric pathology

(i.e., neuroses); (3) they recognized the pharmacological

sensitivity of the vagus to cholinergic agents, thereby

potentially identifying pharmacological treatments; (4) they

brought to the attention of the medical community the

commonality of the vagal innervations of various peripheral

organs and thus a possible common explanation for several

clinical disorders.

2.5. HRV as a psychophysiological variable

Although it might be argued that HRV cannot be studied

without an understanding of the neural regulation of the heart

and the construct of a feedback system, interest in the neural

regulation of the heart was not a major concern during the

founding years of psychophysiology as a discipline. During

these early years two apparently conﬂicting models drove

research in cardiovascular psychophysiology: one, proposed by

Lacey (1967), hypothesized that baroreceptors were involved in

mediating the relation between sensory thresholds and short

latency directional heart rate changes; and the other, proposed

by Obrist (1981), linked heart rate levels to metabolic demands.

Both models emphasized heart rate level and the direction of

beat-to-beat heart rate changes. Variability of heart rate did not

ﬁt within either model. In fact, since early psychophysiology

evolved out of S–R paradigms, heart rate changes were viewed

as dependent variables similar to psychological processes (e.g.,

stimulus detection or attention) consistent with the Lacey

model, or observable behaviors (e.g., reaction time or

movement) consistent with the Obrist model. Within these

prevalent models, HRV could be viewed as error variance due to

poor experimental control. These theoretical positions, if taken

to an extreme, would assume that alterations in heart rate would

be entirely under the control of experimental or environmental

demands. This, of course, is in direct contradiction to our

current knowledge of the dynamic relationship between the

heart and the central nervous system and the inﬂuence of this

interaction on the production of HRV.

Consistent with the descriptive treatment of autonomic

responses in psychophysiology, HRV was introduced as an

operationally deﬁned descriptive variable, similar to an

observable behavior, without neurophysiological attributions.

Early studies quantiﬁed HRV as the variability of beat-to-beat

or second-to-second patterns. Three experimental approaches

were applied: (1) an individual difference model treating HRV

as a trait-like variable similar to ‘‘temperament’’ or a ‘‘clinical

diagnosis’’ variable that predisposes an individual to respond

behaviorally and autonomically with a predictable pattern; (2)

the measurement of changes in HRV as a measure of mental

effort or attention; (3) operant conditioning experiments that

demonstrated that HRV could be placed under stimulus control.

Difﬁculties in conceptualizing HRV as a robust psychophy-

siological variable, were, in part, due to its use as both an

individual difference related to behavioral impulsivity or

physiological reactivity and as a dependent variable sensitive to

sustained attention. Lacey and Lacey (1958) reported that

individuals with greater HRV (i.e., a measure of autonomic

lability) were more behaviorally impulsive. This was preceded

by Eppinger and Hess (1915), who had described a vagotonic

syndrome with clinical features that included an exaggerated

RSA. Consistent with this interest in HRV as an individual

difference variable, Porges (1972, 1973) reported that indivi-

duals with greater baseline HRV had faster reaction times and

expressed larger changes in HRV during an attention task.

Kalsbeek and Ettema (1963) demonstrated a reduction in HRV

during increases in mental load. Lacey (1967) noted, but did not

quantify, that heart rate appeared to stabilize during attention.

Porges and Raskin (1969) quantiﬁed HRV and demonstrated

that HRV was signiﬁcantly depressed during attention

demands. These paradigms were extended to human neonates

and studies conﬁrmed that during sustained stimulus presenta-

tion, HRV was reduced and individual differences in baseline

HRV were correlated with heart rate reactivity (Porges, 1973).

Additionally, studies from the Lang laboratory investigated the

effects of feedback in the regulation of HRV (Hnatiow and

Lang, 1965; Lang et al., 1967). Sayers (1973) introduced

spectral analyses as a method for quantifying HRV during

ergonomic tasks. This was followed by the introduction of

cross-spectral analysis (Porges, 1976) as a strategy to describe

the coupling between respiration and heart rate and the

application of spectral analysis to deﬁne a construct of cardiac

vagal tone (Porges et al., 1981).

S.W. Porges / Biological Psychology 74 (2007) 116–143118

As interest in HRV increased, it was used both as an

individual difference variable in obstetrics, pediatrics, devel-

opmental psychology, psychiatry, and health psychology, and

as a response variable in ergonomics, human factors engineer-

ing, and cognitive sciences. The introduction of HRV required a

shift in theoretical orientation in cardiovascular psychophy-

siology, from a paradigm-bound S–R approach that treated

heart rate patterns as ‘‘behaviors,’’ to an appreciation of both

the neural mechanisms mediating the rhythmic changes in heart

rate and the methodologies needed for quantiﬁcation.

To understand HRV from a neurophysiological perspective, it

is necessary to conceptualize beat-to-beat variability as the

superimposed sum of several rhythmic heart rate oscillations and

slow trends most likely covarying with metabolic demands. Each

prevalent periodic process is assumed to represent a potentially

identiﬁable and quantiﬁable neural feedback circuit mediated by

various mechanisms. The two most reliably described heart rate

periodicities occur at a ‘‘fast’’ frequency associated with

spontaneous breathing (i.e., RSA) and a slower or ‘‘low’’

frequency (LF) assumed to be related to the endogenous rhythm

of blood pressure regulation via the baroreceptors and

spontaneous vasomotor activity. Each periodicity is a product

of a feedback loop, with the period representing the time constant

and the amplitude representing a functional neural input

modulating the cardiac pacemaker. Thus, methodologies from

time series statistics needed to be imported to partition and

decompose the beat-to-beat heart rate signal into constituent

periodic components representing plausible neurophysiological

feedback loops on the cardiac pacemaker.

This change in orientation required a new conceptualization

of the autonomic nervous system that shifted emphasis from

target organs in the periphery to central-peripheral neural

feedback ‘‘circuits.’’ With new models came contradictions of

earlier views of autonomic function. Psychophysiology had

focused on the ‘‘motor’’ component of the autonomic nervous

system, consistent with Langley’s (1921) emphasis on the

motor output of the autonomic nervous system solely as a motor

system. Thus, heart rate, similar to any other observable

behavior, was treated as a ‘‘response.’’ In contrast, a ‘‘system’’

model incorporates an elaboration of feedback mechanisms

from the periphery and central modulators of the output gain of

the efferent pathways. Thus, a systems approach would not only

describe the components of the feedback loop, but would also

attempt to understand the features of central mechanisms

mediating the gain of the output system. In the case of RSA, this

would result in a focus on the features that mediate frequency

and amplitude. In general, the literature demonstrates that the

frequency of RSA is generated by the same brainstem

mechanisms involved in generating the frequency of respira-

tion, while the amplitude of RSA represents the functional

impact of vagal efferent pathways originating in the nucleus

ambiguus on the cardiac pacemaker (Haselton et al., 1992;

Richter and Spyer, 1990; Spyer and Jordan, 1987).

A naı

¨ve treatment of HRV and RSA as output responses

without the consequential inﬂuence of afferent feedback is

consistent with Langley’s (1921) deﬁnition of a limited

autonomic nervous system consisting solely of visceral efferent

ﬁbers and excluding the sensory ﬁbers that accompany most

visceral motor ﬁbers. Although the deﬁnition is often expanded

to include both visceral afferents and central structures (e.g.,

hypothalamus), contemporary textbooks focus on the motor

components, minimizing in their description the important role

of afferent and central contributions to the regulation of the

peripheral autonomic organs. This bias, by ignoring the impor-

tance of the afferent pathways, neglects the feedback and

central regulatory features of a functional system. Moreover, it

limits the study of the dynamic regulatory function of the

autonomic nervous system, since the regulation of visceral state

and the maintenance of homeostasis implicitly assume a

feedback system with the necessary constituent components of

motor, sensory, and regulatory components. Thus, from a

systems perspective, the autonomic nervous system includes

afferent pathways conveying information regarding the visceral

organs and the brain areas (e.g., medulla, hypothalamus) that

interpret the afferent feedback and exert control over the motor

output back to the visceral organs.

3. The polyvagal theory: a phylogenetic theory of

adaptive reactions to challenge

Within this historical context, the polyvagal theory was

presented (Porges, 1995) as an emerging model of neural

regulation of the autonomic nervous system. In the original

presentation (Porges, 1995), the following seven points were

listed to summarize the theory:

(1) The vagal system does not represent a unitary dimension.

(2) There are two vagal motor systems.

(3) In mammals, the concept that vagal tone represents a single

or summed system may have limited physiological or

heuristic value.

(4) The functional output on the heart by the vagal efferent

pathways originating in nucleus ambiguus may be

monitored by RSA.

(5) The magnitude of neurogenetic bradycardia is mediated by

the dorsal motor nucleus.

(6) There is a common cardiopulmonary oscillator.

(7) Primary emotions are related to autonomic function.

Additional points, as listed below, embedded in the theory

have been discussed and expanded in several manuscripts

(Porges, 1995, 1997, 1998, 2001a, 2003):

(1) The phylogenetic development of the neural regulation of

the heart.

(2) The functional and structural distinction between the vagal

efferent pathways originating in the nucleus ambiguus and

the dorsal motor nucleus of the vagus.

(3) The identiﬁcation and adaptive function of three phylo-

genetically ordered neural circuits regulating the heart.

(4) The application of the Jacksonian principle of ‘‘dissolu-

tion’’ to explain the sequencing of the response hierarchy.

(5) A proposed neural process, neuroception, that evaluates risk

and modulates vagal output via higher brain structures.

S.W. Porges / Biological Psychology 74 (2007) 116–143 119

(6) The neuroanatomical and neurophysiological link between

the vagal regulation of the heart and the neural regulation of

the striated muscles of the face and head.

(7) The important role that physiological state, via afferent

feedback to brain structures, has on reactivity to environ-

mental stimuli.

(8) The name polyvagal is used to emphasize the diverse

features of the vagus, that include efferents originating

primarily from two source nuclei in the brainstem and the

prevalence of afferents.

The polyvagal theory provides several insights into the

adaptive nature of physiological state. First, the polyvagal

theory emphasizes that physiological states support different

classes of behavior. For example, a physiological state

characterized by a vagal withdrawal would support the

mobilization behaviors of ﬁght and ﬂight. In contrast, a

physiological state characterized by increased vagal inﬂuence

(via pathways originating in the nucleus ambiguus) on the heart

would support spontaneous social engagement behaviors.

Second, the theory emphasizes the functional and structural

links between neural control of the striated muscles of the face

and the smooth muscles of the viscera. Third, the polyvagal

theory (Porges, 2003) proposes a mechanism, neuroception, to

trigger or to inhibit defense strategies. Neuroception, as a

process, determines whether speciﬁc features in the environ-

ment elicit speciﬁc physiological states that would support

either ﬁght–ﬂight or social engagement behaviors. Neurocep-

tion may involve areas of the temporal cortex that decode

biological movement and detect the intentionality of social

interactions.

The polyvagal theory emphasizes the neurophysiological

and neuroanatomical distinction between two branches of the

vagus and proposes that each branch supports different adaptive

behavioral strategies. The theory (Porges, 1995, 1997, 1998,

2001a, 2003) articulates three phylogenetic stages of the

development of the vertebrate autonomic nervous system (see

Fig. 1). Each stage is associated with a distinct autonomic

subsystem or circuit that is retained and expressed in mammals.

These autonomic subsystems are phylogenetically ordered and

behaviorally linked to social communication (e.g., facial

expression, vocalization, listening), mobilization (e.g., ﬁght–

ﬂight behaviors), and immobilization (e.g., feigning death,

vaso-vagal syncope, and behavioral shutdown). The social

communication system (i.e., social engagement system, see

below) is dependent upon the functions of the myelinated

vagus, which serves to foster calm behavioral states by

inhibiting the sympathetic inﬂuences to the heart and

dampening the HPA axis (e.g., Bueno et al., 1989). The

mobilization system is dependent on the functioning of the

sympathetic nervous system. The most phylogenetically

primitive component, the immobilization system, is dependent

on the unmyelinated or ‘‘vegetative’’ vagus, which is shared

with most vertebrates. With increased neural complexity due to

phylogenetic development, the organism’s behavioral and

affective repertoire is enriched. The three circuits can be

conceptualized as dynamic, providing adaptive responses to

safe, dangerous, or life-threatening events and contexts.

The three circuits are organized and respond to challenges in

a phylogenetically determined hierarchy consistent with the

Jacksonian principle of dissolution. Jackson proposed that in

the brain, higher (i.e., phylogenetically newer) neural circuits

inhibited lower (i.e., phylogenetically older) neural circuits and

‘‘when the higher are suddenly rendered functionless, the lower

rise in activity’’ (Jackson, 1958). Although Jackson proposed

dissolution to explain changes in nervous system function due

to damage and illness, the polyvagal theory proposes a similar

phylogenetically ordered hierarchical model to describe the

sequence of autonomic response strategies to challenges.

Functionally, when the environment is perceived as safe, two

important features are expressed. First, the bodily state is

regulated in an efﬁcient manner to promote growth and

restoration (e.g., visceral homeostasis). This is done through an

increase in the inﬂuence of myelinated vagal motor pathways

on the cardiac pacemaker that slows the heart, inhibits the ﬁght/

ﬂight mechanisms of the sympathetic nervous system, dampens

the stress response system of the HPA-axis (e.g., cortisol), and

reduces inﬂammation by modulating immune reactions (e.g.,

cytokines). Second, through the process of evolution, the

brainstem nuclei that regulate the myelinated vagus became

integrated with the nuclei that regulate the muscles of the face

and head. This link results in the bi-directional coupling

between spontaneous social engagement behaviors and bodily

states. Speciﬁcally, the visceral states that promote growth and

S.W. Porges / Biological Psychology 74 (2007) 116–143120

Fig. 1. Phylogenetic stages of the polyvagal theory.

restoration are linked neuroanatomically and neurophysiologi-

cally with the muscles that regulate eye gaze, facial expression,

listening, and prosody (see Porges, 2001a for review).

The human nervous system, similar to other mammals, did

not evolve solely to survive in safe environments, but also to

promote survival in dangerous and life-threatening contexts. To

accomplish this adaptive ﬂexibility, the human nervous system

retained two more primitive neural circuits to regulate

defensive strategies (i.e., ﬁght/ﬂight and freeze behaviors). It

is important to note that social behavior, social communication,

and visceral homeostasis are incompatible with the neurophy-

siological states and behaviors promoted by the two neural

circuits that support defense strategies. Thus, via evolution, the

human nervous system retains three neural circuits, which are

in a phylogenetically organized hierarchy. In this hierarchy of

adaptive responses, the newest circuit is used ﬁrst, and if that

circuit fails to provide safety, the older circuits are recruited

sequentially.

By investigating the phylogeny of the regulation of the

vertebrate heart (Morris and Nilsson, 1994; Porges, 1995, 1997;

Taylor et al., 1999), four principles can be extracted that

provide a basis for speculations regarding the neural mechan-

isms underlying social engagement, as well as ﬁght–ﬂight and

freeze behaviors:

(1) There is a phylogenetic shift in the regulation of the heart

from endocrine communication, to unmyelinated nerves,

and ﬁnally to myelinated nerves.

(2) There is a development of opposing neural mechanisms of

excitation and inhibition to provide rapid regulation of

graded metabolic output.

(3) A face–heart connection evolved as source nuclei of vagal

pathways shifted ventrally from the older dorsal motor

nucleus to the nucleus ambiguus. This resulted in an

anatomical and neurophysiological linkage between the

neural regulation of the heart via the myelinated vagus and

the special visceral efferent pathways that regulate the

striated muscles of the face and head.

(4) With increased cortical development, the cortex exhibits

greater control over the brainstem via direct (e.g.,

corticobulbar) and indirect (e.g., corticoreticular) neural

pathways originating in motor cortex and terminating in the

source nuclei of the myelinated motor nerves emerging

from the brainstem (e.g., speciﬁc neural pathways

embedded within cranial nerves V, VII, IX, X, XI),

controlling visceromotor structures (i.e., heart, bronchi,

thymus) and somatomotor structures (muscles of the face

and head).

The polyvagal theory proposes that the evolution of the

mammalian autonomic nervous system provides the neuro-

physiological substrates for the emotional experiences and

affective processes that are major components of social

behavior. The theory proposes that physiological state limits

the range of behavior and psychological experience. In this

context, the evolution of the nervous system determines the

range of emotional expression, quality of communication, and

the ability to regulate bodily and behavioral state. The

polyvagal theory links the evolution of the autonomic nervous

system to affective experience, emotional expression, facial

gestures, vocal communication, and contingent social behavior.

Thus, the theory provides a plausible explanation of several

social, emotional, and communication behaviors and disorders.

3.1. The vagal brake

Unique to mammals, the primary vagal regulation of the

heart shifted from the unmyelinated pathways originating in the

dorsal motor nucleus of the vagus to include myelinated

pathways originating in the nucleus ambiguus. The myelinated

vagus functions as an active vagal brake (see Porges et al.,

1996), in which rapid inhibition and disinhibition of vagal tone

to the heart can rapidly mobilize or calm an individual. The

myelinated vagus actively inhibits the sympathetic nervous

system’s inﬂuences on the heart and dampens hypothalamic-

pituitary adrenal (HPA) axis activity (see Porges, 2001a).

Functionally, the vagal brake, by modulating visceral state,

enables the individual to rapidly engage and disengage with

objects and other individuals and to promote self-soothing

behaviors and calm states. Developmentally, the number of

myelinated vagal ﬁbers increases linearly from 24 to 28 weeks

gestation until full-term birth, when the number of ﬁbers is

comparable to those observed in adolescence (Sachis et al.,

1982). In full-term infants, the myelination process is active

during the ﬁrst year of life, particularly during the ﬁrst 3 months

(Pereyra et al., 1992). Thus, deﬁcits in the regulation of the

vagal brake may be causal in deﬁcits in social communication

observed early in development. Basically, the expression of

social engagement behaviors is dependent upon the regulation

of visceral state by the vagal brake. If visceral homeostasis is

challenged and the vagal brake is unable to regulate visceral

state, then social engagement behaviors will be minimized.

Thus, it is possible that psychiatric disorders, (e.g., autism,

schizophrenia, reactive attachment disorder) in which com-

promised social behaviors are diagnostic features, are

associated with neurobiological state regulation strategies that

foster defensive and not social behaviors.

The mammalian heart is characterized by a relatively strong

vagal inﬂuence, via the myelinated pathways, on the heart’s

pacemaker (i.e., sino-atrial node). Due to the tonic vagal

inﬂuences on the sino-atrial node, resting heart rate is substan-

tially lower than the intrinsic rate of the pacemaker. Even within

mammals, there are large species differences in RSA, and

these differences may be related to species-typical behavioral

repertoire and afﬁliative social behavior (Grippo et al., in press).

When the vagal tone to the pacemaker is high, the vagus acts as a

restraint or brake, limiting the rate at which the heart is beating.

When vagal tone to the pacemaker is low, there is little or no

inhibition of the pacemaker. Thus, the brake metaphor is a useful

construct to describe the functional modulation of heart rate by

the myelinated vagal efferent pathways. The vagal brake

provides a neural mechanism to rapidly change visceral state

by slowing or speeding heart rate. Consistent with the assump-

tions of the polyvagal theory, the vagal brake contributes to the

modulation of cardiac output by decreasing the inhibitory vagal

S.W. Porges / Biological Psychology 74 (2007) 116–143 121

control of the heart to speed heart rate and by increasing the

inhibitory vagal control of the heart to slow heart rate. Thus,

neurophysiologically, the vagal brake is removed or reduced to

support the metabolic requirements for mobilization and

maintained or increased to support social engagement behaviors.

Although there are several mechanisms to modulate heart rate,

only the myelinated vagal efferent pathways, via nicotinic

preganglionic receptors on the sino-atrial node, are capable of the

rapid instantaneous changes that characterize RSA (see Cheng

and Powley, 2000).

Although the vagus inﬂuences the heart in other vertebrates

(for review, see Taylor et al., 1999), RSA and the vagal brake

are constructs that are used in this paper to refer only to the

unique characteristics of the myelinated vagus in the

mammalian autonomic nervous system. Speciﬁcally, RSA is

proposed as a portal, allowing accurate measurement of the

dynamic inﬂuence of myelinated vagal efferent pathways on

the sino-atrial node. Consistent with the polyvagal theory,

measurement of the dynamic function of the vagal brake, via

accurate quantiﬁcation of RSA, provides a continuous measure

of functional inﬂuence of the myelinated vagus on the heart.

Neurophysiologically, the vagal brake is removed or reduced

to support the metabolic requirements for mobilization (e.g.,

associated with ﬁght/ﬂight behaviors) and maintained or

increased to support social engagement behaviors. Measurement

of the amplitude of RSA provides an assessmentof the state of the

vagal brake. Thus, the polyvagal theory frames a research

agenda, by proposing that the vagal brake is related to behavioral

and psychological processes along a continuum, from prosocial–

afﬁliative interactions to adaptive ﬁght/ﬂight behaviors.

RSA is a naturally occurring rhythm in the heart rate pattern

at approximately the frequency of spontaneous breathing. The

amplitude of RSA can be quantiﬁed to provide a sensitive index

of the impact of the myelinated vagus on the heart (Porges,

1995). By assessing RSA during various challenges, it is

possible to measure the dynamic regulation of the vagal brake.

The amplitude of RSA is not constant and varies as a function of

experimental conditions in which behavioral and psychological

demands are manipulated. The sensitivity of RSA to context

and task demands creates a statistical problem, since RSA data

tend not to be statistically stationary, although the traditional

statistical methodologies used to quantify RSA (e.g., spectral

analysis, peak–trough) assume stationarity. To deal with this

speciﬁc statistical challenge, our laboratory developed an

innovative methodology to remove the non-stationary trends

and slow periodic processes via a moving polynomial

procedure (see Bohrer and Porges, 1982; Porges, 1985; Porges

and Bohrer, 1990; Porges and Byrne, 1992).

3.2. RSA and behavioral regulation

The literature consistently supports the model relating

autonomic state to social engagement behaviors and emotion

regulation proposed in the polyvagal theory. First, the literature

supports the hypothesis that a high level and, to a greater extent,

reliable suppression of RSA are ‘‘positive’’ indices of social

and emotional regulation. In contrast, low levels and unreliable

RSA modulation appear to be ‘‘risk’’ indices for difﬁculties in

social and emotional regulation and, in some studies, associated

with psychiatric disorders. Second, current research being

conducted in our laboratory links individual differences in

facial expressivity (i.e., facial EMG) to individual differences

in RSA, with low amplitude RSA covarying with low muscle

tone to the upper face.

Several laboratories report that children with behavioral

regulation problems have lower baseline RSA and dampened

RSA responses during testing sessions (see Calkins, 1997;

Porges et al., 1996; Blair and Peters, 2003). Calkins and Keane

(2004) reported that children with stable RSA suppression

across the preschool period were less emotionally negative and

had fewer behavior problems and better social skills than other

children. RSA suppression in children has been reported to

moderate social stress within the family and with peers. Only in

children who did not suppress RSA was hostile-withdrawn

parenting associated with higher levels of peer conﬂict (Leary

and Katz, 2004). The speciﬁcity of the vagal branch of the

autonomic nervous system in mediating affect was observed in

24-month olds who suppressed RSA, independent of cardiac

pre-ejection period, a measure of sympathetic tone (see

Berntson et al., 1994), with increasing distress across negative

emotion tasks (Buss et al., 2005).

In preschool aged children, higher baseline RSA is

correlated with greater emotional expressivity (see Cole

et al., 1996). Adolescent brothers of adjudicated delinquents

with higher RSA were at reduced risk for delinquency and

externalizing psychopathology (see Pine et al., 1998). Katz and

Gottman (1995) report that high RSA buffers the child from the

effects of marital hostility. In adults, higher RSA predicts

greater self-reported regulatory control and decreased negative

emotional arousal in response to stressors (Fabes and

Eisenberg, 1997). Kennedy et al. (2004) reported that young

children with higher RSA moderated maternal restrictive-

parenting practices, while mothers of children with lower RSA

were more likely to report restrictive parenting practices.

In adults, poorer modulation of RSA was associated with

greater social anxiety, and lower RSA was associated with

greater defensiveness (Movius and Allen, 2005). Clinically

anxious subjects exhibit lower and less suppression of RSA

(Lyonsﬁeld et al., 1995; Friedman and Thayer, 1998). RSA

level appears to parallel the positive effects of treatment, with

increases in RSA being reported only in patients with

depression who exhibited a clinically signiﬁcant response to

treatment (Chambers and Allen, 2002). Greater RSA suppres-

sion to sad video clips has been reported to predict recovery

from depression (Rottenberg et al., 2005). A recent study with

borderline personality disorder (Austin et al., in press)

illustrates how measures of the dynamic regulation of the

vagal brake can provide insight into the behavioral and affective

features of the disorder. Although initial levels of RSA in the

borderline group were similar to controls, during the

experiment (i.e., ﬁlm clips varying in emotional content), the

borderline and control groups had different trajectories. RSA

progressively decreased in the borderline group, while RSA

progressively increased in the control group. By the end of the

S.W. Porges / Biological Psychology 74 (2007) 116–143122

experiment, the groups differed signiﬁcantly on both RSA and

heart rate. The correlation between the changes in RSA and heart

rate was signiﬁcant only for the control group. These ﬁndings

suggest that vagal mechanisms mediated the heart rate slowing in

the control group, but did not mediate the heart rate speeding in

the borderline group. Perhaps these ﬁndings implicated a

sympathetic mechanism, as proposed in the polyvagal theory,

that is potentiated only during states when the inﬂuence of the

vagal brake is reduced. Consistent with this interpretation of a

vulnerable state characterized by reduced inﬂuence of the vagal

brake, others have reported that health factors, including

cardiovascular risk (Hayano et al., 1990) and diabetes and

obesity (Quilliot et al., 2001), are related to low RSA.

3.3. The social engagement system: phylogenic integration

of behavioral and autonomic components

The phylogenic origin of the behaviors associated with the

social engagement system is intertwined with the phylogeny of

the autonomic nervous system. As the muscles of the face and

head emerged as social engagement structures, a new component

of the autonomic nervous system (i.e., a myelinated vagus)

evolved that was regulated by the nucleus ambiguus, a medullary

nucleus ventral to the dorsal motor nucleus of the vagus. This

convergence of neural mechanisms produced an integrated social

engagement system with synergistic behavioral (i.e., somato-

motor) and visceral components, as well as interactions among

ingestion, state regulation, and social engagement processes.

The neural pathways originating in several cranial nerves

that regulate the striated muscles of the face and head (i.e.,

special visceral efferent) and the myelinated vagal ﬁbers form

the neural substrate of the social engagement system (see

Porges, 1998, 2001a, 2003). As illustrated in Fig. 2, the

somatomotor component includes the neural structures

involved in social and emotional behaviors. Special visceral

efferent nerves innervate striated muscles, which regulate the

structures derived during embryology from the ancient gill

arches (Truex and Carpenter, 1969). The social engagement

system has a control component in the cortex (i.e., upper motor

neurons) that regulates brainstem nuclei (i.e., lower motor

neurons) to control eyelid opening (e.g., looking), facial

muscles (e.g., emotional expression), middle ear muscles (e.g.,

extracting human voice from background noise), muscles of

mastication (e.g., ingestion), laryngeal and pharyngeal muscles

(e.g., prosody and intonation), and head turning muscles (e.g.,

social gesture and orientation). Collectively, these muscles

function both as determinants of engagement with the social

environment and as ﬁlters that limit social stimuli. The neural

pathways that raise the eyelids also tense the stapedius muscle

in the middle ear, which facilitates hearing human voice. Thus,

the neural mechanisms for making eye contact are shared with

those needed to listen to human voice. As a cluster, difﬁculties

in gaze, extraction of human voice, facial expression, head

gesture and prosody are common features of individuals with

autism and other psychiatric disorders.

There are interneuronal connections between the source

nuclei (i.e., lower motor neurons) of special visceral efferent

pathways and the source nucleus of the myelinated vagus. These

neurophysiological circuits provide an inhibitory pathway to

slow heart rate and lower blood pressure, which, by actively

reducing autonomic arousal, promotes the calm states necessary

to express social engagement behaviors and to support health,

growth, and restoration. The brainstem source nuclei of this

system are inﬂuenced by higher brain structures and by visceral

afferents. Direct corticobulbar pathways reﬂect the inﬂuence of

frontal areas of the cortex (i.e., upper motor neurons) on the

medullary source nuclei of this system. Moreover, feedback

through the afferent vagus (e.g., tractus solitarius) to medullary

areas (e.g., nucleus of the solitary tract) inﬂuences both the

source nuclei of this system and the forebrain areas that are

assumed to be involved in several psychiatric disorders (e.g.,

Craig, 2005; Thayer and Lane, 2000). In addition, the anatomical

structures involved in the social engagement system have

neurophysiological interactions with the HPA axis, the social

neuropeptides (e.g., oxytocin and vasopressin), and the immune

system (for overview, see Carter, 1998; Porges, 2001b).

Afferents from the target organs of the social engagement

system, including the muscles of the face and head, provide

potent afferent input to the source nuclei regulating both the

visceral and somatic components of the social engagement

system. Thus, activation of the somatomotor component (e.g.,

listening, ingestion, lifting eyelids) could trigger visceral

changes that would support social engagement, while

modulation of visceral state, depending on whether there is

an increase or decrease in the inﬂuence of the myelinated vagal

efferents on the sino-atrial node (i.e., increasing or decreasing

the inﬂuence of the vagal brake), would either promote or

impede social engagement behaviors. For example, stimulation

of visceral states that would promote mobilization (i.e., ﬁght or

ﬂight behaviors) would impede the ability to express social

engagement behaviors.

S.W. Porges / Biological Psychology 74 (2007) 116–143 123

Fig. 2. The social engagement system. Social communication is determined by

the cortical regulation of medullary nuclei via corticobulbar pathways. The

social engagement system consists of a somatomotor component (i.e., special

visceral efferent pathways that regulate the striated muscles of the face and

head) and a visceromotor component (i.e., the myelinated vagus that regulates

the heart and bronchi). Solid blocks indicate the somatomotor component.

Dashed blocks indicate the visceromotor component.

The polyvagal theory provides an explicit neurobiological

model linking difﬁculties in spontaneous social behavior to

both facial expressivity and the regulation of visceral state.

Alternatively, the theory describes mechanisms through which

social behaviors may serve as regulators of physiological

activity and vice versa. The theory also proposes plausible

mechanisms through which visceral states might form a core

domain of several psychiatric proﬁles. Relevant to this focus on

psychiatric disorders are the speciﬁc deﬁcits, associated with

several diagnoses, in both the somatomotor (e.g., poor gaze,

low facial affect, lack of prosody, difﬁculties in mastication)

and visceromotor (difﬁculties in autonomic regulation resulting

in cardiopulmonary and digestive problems) components of the

social engagement system. For example, clinicians and

researchers have documented these deﬁcits in individuals with

autism spectrum disorders. Deﬁcits in the social engagement

system would compromise spontaneous social behavior, social

awareness, affect expressivity, prosody, and language devel-

opment. In contrast, interventions that improve the neural

regulation of the social engagement system, hypothetically

would enhance spontaneous social behavior, state and affect

regulation, reduce stereotypical behaviors, and improve vocal

communication (i.e., including enhancing both prosody in

expressive speech and the ability extract human voice from

background sounds).

Sound in our environment impinges on the eardrum and

causes it to vibrate. These vibrations are transduced from the

eardrum to the inner ear via the small bones in the middle ear

known as ossicles. The stapedius muscle (innervated via a

branch of the facial nerve) and the tensor tympani (innervated

via a branch of the trigeminal nerve), when innervated, stiffen

the ossicular chain and dampen the amplitude of the low

frequency sounds reaching the inner ear. The functional impact

of these muscles on the perceived acoustic environment is to

markedly attenuate low frequency sounds and to facilitate the

extraction of high frequency sounds associated with human

voice. For example, our acoustic environment is often

dominated by loud low frequency sounds that have the

functional effect of masking the soft high frequency sounds

associated with human voice. In humans, the ossicular chain is

regulated primarily by the stapedius muscle, and tensing the

stapedius prevents this masking effect (see Borg and Counter,

1989). In fact, individuals who can voluntarily contract middle

ear muscles exhibit an attenuation of approximately 30 dB at

frequencies below 500 Hz, while there is no or minimal

attenuation at frequencies above 1000 Hz (see Kryter, 1985).

The structures at the end of the mandible (i.e., jaw bone) that

deﬁne components in the middle ear became detached during

the phylogenetic transition from reptiles to mammals (Luo

et al., 2001; Rowe, 1996; Wang et al., 2001). It has been

proposed that this detachment overcame a structural restriction

that allowed the cranium to expand in mammals. With the

evolution of a neural system that regulated the ossicles, low

amplitude, relatively high frequency, airborne sounds (i.e.,

sounds in the frequency band of human voice) could be heard,

even when the acoustic environment was dominated by low

frequency sounds.

Studies have demonstrated that the neural regulation of

middle ear muscles is defective in individuals with language

delays, learning disabilities and autism spectrum disorders

(Smith et al., 1988; Thomas et al., 1985). Middle ear infection

(i.e., otitis media) may result in a total inability to elicit the

‘‘reﬂexive’’ contraction of the stapedius muscles (Yagi and

Nakatani, 1987). Disorders that inﬂuence the neural function of

the facial nerve (i.e., Bell’s Palsy), not only inﬂuence the

stapedius reﬂex (Ardic et al., 1997), but also affect the patient’s

ability to discriminate speech (Wormald et al., 1995). Thus, the

observed difﬁculties that individuals with language difﬁculties

(e.g., language delay, autism, etc.) have in extracting human

voice from background sounds may be dependent on the same

neural system that regulates facial expression (i.e., the social

engagement system).

3.4. Disorders of the social engagement system:

maladaptive or adaptive behavioral strategies?

Several psychiatric and behavioral disorders are char-

acterized as having difﬁculties in establishing and maintain-

ing social relations. Diagnostic features often include

difﬁculties both in expressing social behavior and in reading

social cues (i.e., social awareness). These features are

observed in a variety of psychiatric diagnoses, including

autism, social anxiety, posttraumatic stress disorder, and

reactive attachment disorder.

Although a compromised social engagement system results

in ‘‘maladaptive’’ social behavior, do these asocial behavioral

strategies have ‘‘adaptive’’ features? The phylogeny of the

vertebrate autonomic nervous system serves as a guide to

understand these adaptive features. Phylogenetically, the

vertebrate autonomic nervous system follows three general

stages of development. In the mammalian autonomic nervous

system, the structures and circuits representing each of the

stages remain, but have been co-opted for various adaptive

functions. The neural circuit associated with each stage

supports a different category of behavior, with the phylogen-

etically most recent innovation (i.e., the myelinated vagus)

capable of supporting high levels of social engagement

behavior. Since the neural regulation of the myelinated vagus is

integrated into the social engagement system, when the social

engagement system is compromised, the effects are both

behavioral and autonomic. The resultant changes in autonomic

state support a range of adaptive defensive behaviors.

Speciﬁcally, the compromised social engagement system

(see Fig. 2) is associated, neurophysiologically, with a change

in autonomic regulation characterized by a reduction in the

inﬂuence of the myelinated vagus on the heart. The removal of

the regulatory inﬂuence of the myelinated vagus on the heart

potentiates the expression of the two phylogenetically older

neural systems (i.e., sympathetic nervous system, unmyeli-

nated vagus). These two older neural systems foster

mobilization behaviors of ﬁght and ﬂight, via the sympathetic

nervous system, or immobilization behaviors of death

feigning, freezing, and behavioral shut down via the

unmyelinated vagus.

S.W. Porges / Biological Psychology 74 (2007) 116–143124

3.5. Neuroception

To effectively switch from defensive to social engagement

strategies, the mammalian nervous system needs to perform two

important processes: (1) to assess risk, and (2) if the environment

is perceived as safe, to inhibit the more primitive limbic

structures that control ﬁght, ﬂight, or freeze behaviors. The

nervous system, through the processing of sensory information

from the environment (and viscera), continuously evaluates risk.

Since the neural evaluation of risk does not require conscious

awareness and may involve subcortical limbic structures (e.g.,

Morris et al., 1999), the term neuroception was introduced to

emphasize a neural process, distinct from perception, that is

capable of distinguishing environmental (and visceral) features

that are safe, dangerous, or life threatening. In safe environments,

autonomic state is adaptively regulated to dampen sympathetic

activation and to protect the oxygen dependent central nervous

system, and especially the cortex, from the metabolically

conservative reactions of the dorsal vagal complex. However,

how does the nervous system know when the environment is safe,

dangerous, or life threatening, and what neural mechanisms

evaluate this risk?

Neuroception might involve feature detectors in the

temporal cortex (see below), since these structures respond

to familiar voices and faces and hand movements and inﬂuence

limbic reactivity. In most individuals (i.e., without a psychiatric

disorder or neuropathology), the nervous system evaluates risk

(i.e., neuroception) and matches neurophysiological state with

the actual risk of the environment. When the environment is

appraised as being safe, the defensive limbic structures are

inhibited, enabling social engagement and calm visceral states.

In contrast, some individuals experience a mismatch, and the

nervous system appraises the environment as being dangerous,

when it is safe. This mismatch results in physiological states

that support ﬁght, ﬂight, or freeze behaviors, but not social

engagement behaviors. According to the theory, social

communication can be expressed efﬁciently through the social

engagement system, only when these defensive circuits are

inhibited. Neuroception represents a neural process that enables

mammals to engage in social behaviors by distinguishing safe

from dangerous contexts. Neuroception is proposed as a

plausible mechanism mediating both the expression and the

disruption of positive social behavior, emotion regulation, and

visceral homeostasis.

New technologies, such as fMRI, have identiﬁed speciﬁc

neural structures that are involved in detecting risk. The

temporal lobe is of particular interest in expanding the construct

of neuroception and in identifying neural mechanisms that, by

detecting and evaluating risk, modulate the expression of

adaptive defensive behaviors and autonomic states. Functional

imaging techniques document that areas of the temporal cortex,

fusiform gyrus, and superior temporal sulcus are involved in

evaluating biological movement and intention, including the

detection of features such as movements, vocalizations, and

faces, which contribute to an individual being perceived as safe

or trustworthy (Adolphs, 2002; Winston et al., 2002). Slight

changes in these stimuli can pose threat or signal endearment.

Connectivity between these areas of the temporal cortex and the

amygdala suggests a top–down control in the processing of

facial features that could inhibit activity of the structures

involved in the expression of defensive strategies (Pessoa et al.,

2002).

Neuroanatomical and neurophysiological research with

animals provides additional information regarding the modula-

tion and inhibition of defensive behaviors via well-deﬁned

connections among the amygdala, the periaqueductal gray

(PAG), and the autonomic nervous system. The PAG is a

heterogeneous midbrain structure that consists of gray matter

surrounding the cerebral aqueduct that connects the third and

fourth ventricles. Studies have identiﬁed areas of the PAG that

are organized to regulate ﬂight, ﬁght, or freeze behaviors and

the autonomic states that support these behaviors (Keay and

Bandler, 2001). Stimulating rostrally within the lateral and

dorsolateral PAG produces confrontational defensive behaviors

(i.e., ﬁght), while stimulating caudally within the lateral PAG

and dorsolateral PAG produces escape behaviors (i.e., ﬂight).

Autonomic shifts such as increases in heart rate and blood

pressure parallel these behaviors. In contrast, stimulation in the

region of the PAG ventrolateral to the aqueduct (vlPAG) evokes

a passive reaction of immobility, a drop in blood pressure, and a

slowing of heart rate. Interestingly, excitation of the vlPAG

evokes an opioid-mediated analgesia that might adaptively

raise pain thresholds. In addition, there is evidence of a

functional connection between the central nucleus of the

amygdala and the vlPAG that modulates both antinociception

and immobilization (Leite-Panissi et al., 2003). Consistent with

the polyvagal theory, the vlPAG communicates with the dorsal

vagal complex, while the lPAG and dlPAG communicate with

the sympathetic nervous system.

The detection of safety subdues the adaptive defensive

systems dependent on limbic structures. This may provide a

plausible model through which a neural detection of risk (i.e.,

neuroception) would modulate behavioral and physiological

states to support adaptive behaviors in response to safe,

dangerous, or life-threatening environments. In the absence of

threat, inhibitory projections from the fusiform gyrus and the

superior temporal sulcus to the amygdala would be available to

actively inhibit the limbic defense systems. This inhibition

would provide an opportunity for social behavior to emerge.

Thus, the appearance of a friend or mate would subdue the

limbic activation with the biobehavioral consequences of

allowing proximity, physical contact, and other social engage-

ment behaviors. In contrast, during situations in which the

appraisal of risk is high, the amygdala and various areas of the

PAG are activated. The amygdala and PAG only share

connections through the central nucleus of the amygdala

(Rizvi et al., 1991).

Based on the relative risk of the environment, both social

engagement and defense behaviors may be interpreted as either

adaptive or maladaptive. For example, the inhibition of defense

systems by the social engagement system would be adaptive and

appropriate only in a safe environment. From a clinical

perspective, it would be the inability to inhibit defense systems

in safe environments (e.g., anxiety disorders, reactive attachment

S.W. Porges / Biological Psychology 74 (2007) 116–143 125

disorder) or the inability to activate defense systems in risk

environments (e.g., Williams syndrome) that might contribute to

the deﬁning features of psychopathology. Thus, an invalid

neuroception of safety or danger might contribute to maladaptive

physiological reactivity and the expression of the defensive

behaviors associated with speciﬁc psychiatric disorders, that

include in their diagnostic criteria a social deﬁcit (e.g., autism,

social anxiety, Williams syndrome) or fear (e.g., various phobias,

obsessive-compulsive disorder) (Leckman et al., 1997). How-

ever, in most individuals, neuroception accurately reﬂects risk

and there is a consistency between the cognitive awareness of risk

and the visceral response to risk.

3.6. Co-opting the immobilization defense system for

reproductive behaviors, nursing, and the formation of

social bonds

Immobilization, as a defense system, is phylogenetically old

and is associated with reduced metabolic demands and increased

pain threshold. In reptiles, with a larger tolerance for reductions

in oxygen, immobilization is a very effective defense strategy. In

contrast, since mammals have a great need for oxygen, the

inhibition of movement coupled with a shift in autonomic state to

support the immobilization behavior (i.e., apnea and bradycar-

dia) can be lethal (Hofer, 1970; Richter, 1957). However, several

aspects of mammalian social behavior require immobilization,

but immobilization without fear. Immobilization without fear is

accomplished by co-opting the structures that regulate immo-

bilization to serve a broad range of social needs, including

reproduction, nursing, and pair-bonding. By focusing on the area

of the PAG that coordinates freezing behavior, the primitive

immobilization defense system has been modiﬁed in mammals to

serve the intimate social needs of mammals. In addition, it has

been reported that the vlPAG is rich in receptors for oxytocin, a

neuropeptide associated with partuition, nursing, and the

establishment of pair bonds (Carter, 1998; Insel and Young,

2001).

Overlapping with the area of the PAG that organizes

immobility (i.e., vlPAG) are areas that, when stimulated,

produce lordosis and kyphosis. The lordosis reﬂex is a

hormone-dependent behavior displayed by female rodents and

other mammalian species during mating. In most mammals,

lordosis involves the female immobilizing in a crouching

posture with her hind end available to the male for copulation.

Neural tracing studies have demonstrated that the vlPAG is

part of the neural circuit involved in regulating lordosis

(Daniels et al., 1999). Kyphosis is an upright arched back

posture that is accompanied by inhibition of limb movements.

Kyphosis is stimulated by nipple attachment and provides an

opportunity for the dam to feed simultaneously a large litter.

When dams initiate a nursing bout, behavioral state shifts

immediately from high activity to immobility (Stern, 1997).

When the caudal portion of the vlPAG is lesioned there are

important consequences: (1) kyphotic nursing decreases, (2)

litter weight gains decrease, and (3) the lesioned rats are more

aggressive and more frequently attack strange males (Lonstein

and Stern, 1998).

3.7. Polyvagal theory: limitations and expanding

explanations

The polyvagal theory provides neurophysiological organiz-

ing principles to interpret and to test hypotheses relating

peripheral cardiovascular state to the psychological processes

that have intrigued psychophysiologists (e.g., emotion, social

engagement, ﬁght–ﬂight, face-to-face communication). The

theory emphasizes that physiological state limits the range of

social behavior and the ability to regulate emotion. Thus,

creating states of calmness and exercising the neural regulation

of the striated muscles of the face and head may potentiate

positive social behavior by stimulating the neural regulation of

the social engagement system.

The polyvagal theory does not propose that the vagus is the

ultimate cause of individual differences in social engagement

behaviors or emotional regulation. The efferent vagal pathway

originating in the nucleus ambiguus (i.e., manifested in RSA) is

one of several output systems related to emotion and social

engagement behaviors. In the polyvagal theory, the source

nuclei of the myelinated vagus are regulated by complex neural

circuits, involving both visceral afferents and higher brain

structures that inﬂuence the brainstem source nuclei controlling

both the myelinated vagus and the striated muscles of the face

and head (i.e., the social engagement system).

Speciﬁc central pathways from cortical and subcortical areas

(involving the temporal cortex, central nucleus of the

amygdala, and periaqueductal gray) are involved in the

regulation of both the vagal component and somatomotor

component of the social engagement system. Consistent with

the polyvagal theory, others have proposed direct neural

pathways that integrate emotional activity with central

structures that inﬂuence autonomic function (see Phillips

et al., 2003a,b; Thayer and Lane, 2000; Craig, 2005). The

asymmetry of higher brain structures may also play a role in

linking speciﬁc affective experiences with autonomic states.

Consistent with the views that the right hemisphere appears to

play a greater role in affect, especially the adaptive expression

of negative affect (e.g., Canli et al., 1998; Fox, 1991; Noesselt

et al., 2005; Simon-Thomas et al., 2005), the right hemisphere

also appears to have a greater role in regulation of cardiac

function, presumably via shifts in vagal regulation (Ahern et al.,

2001; Porges et al., 1994). Although not the focus of the current

paper, these central structures and their asymmetrical inﬂuence

on autonomic function would be likely candidates to be

involved in the hypothetical process of neuroception described

above.

Most research evaluating autonomic nervous system

activity and psychopathology has used designs contrasting

depressed or anxious groups with control groups. Whether

autonomic dysfunction or atypical autonomic regulation is

causal is not established. However, in a prospective study,

depressed individuals, who subsequently recovered from

depression, reacted with a greater vagal (RSA) withdrawal

to a sad video clip that those that did not recover (i.e.,

Rottenberg et al., 2005). Moreover, as Chambers and Allen

(2002) have reported, RSA appears to parallel the positive

S.W. Porges / Biological Psychology 74 (2007) 116–143126

effects of treatment, with increases in RSA being reported only

in patients who exhibited a clinically signiﬁcant response to

treatment (Chambers and Allen, 2002). Reduced RSA

associated with depression has been hypothesized to produce

clinically signiﬁcant cardiac events related to cardiovascular

disease (Sloan and Bigger, 1991). This inﬂuence might occur

through a top–down modulation of the brainstem centers

regulating the baroreceptors, and result in increased blood

pressure lability. Animal research supports the importance of

projections from the medial prefrontal cortex to the nucleus of

the solitary tract (i.e., the source nucleus of the afferent vagus)

in modulating autonomic state by cortico-solitary projections

regulating the baroreﬂex (Owens et al., 1999).

The polyvagal theory leads to theory-driven research that

will provide a plausible neurobiological foundation for the

explanation and assessment of variants of social-emotional

behavior and disorders, including the compromised social

behavior observed during physical illness and psychiatric

disorders. The polyvagal theory supports research that breaks

the tradition of single variable psychophysiological research,

by identifying theoretically relevant variables involved in the

regulation of social engagement behaviors. In addition, the

theory provides a neurophysiological basis for understanding

several relevant issues in health psychology, including the

beneﬁts of social support and face-to-face communication on

visceral regulation and health. Perhaps most relevant to

psychophysiology as a science, the theory leads to testable

hypotheses that will, in turn, result in modiﬁcations to the

theory.

4. The polyvagal perspective

4.1. Levels of inquiry

Imbedded in the polyvagal theory is a generalizable and

expansive perspective of inquiry. What are the features of this

perspective? How does this perspective inﬂuence the con-

ceptualization of research questions and paradigms in

psychophysiology? The polyvagal perspective reﬂects a level

of inquiry that emphasizes neurophysiological mechanisms and

neurobiological organizing principles to determine how heart

rate measures, as non-invasive features of adaptive neural

circuits, are related to psychological, behavioral, and health

processes. The approach seeks to understand the ‘‘why’’ and

‘‘how’’ of the observed relations between heart rate variables

and psychological, behavioral, and clinical processes. From this

perspective, the polyvagal theory is pragmatically ﬂuid as

knowledge regarding the ‘‘why’’ and ‘‘how’’ of neurophysio-

logical regulation of the autonomic nervous system expands.

Cardiovascular psychophysiology is inﬂuenced by theories,

assumptions, and methodological biases. Often clusters of ideas

and traditions within a discipline form assumed, but untested,

‘‘discipline myths’’ that drive or limit a research agenda.

‘‘Discipline myths’’ often include information that, while

accurate on a descriptive level, is naı

¨ve on other levels of

inquiry. Levels of inquiry drive different questions. These

questions lead to different paradigms. Embedded within each

paradigm are implicit assumptions regarding the mechanisms

mediating heart rate parameters and how these parameters are

related to cognitive, affective, or health variables.

Within the discipline of psychophysiology, heart rate and

HRV traditionally have been treated as ‘‘operationally’’ deﬁned

dependent variables, similar to behavior. Within the discipline of

physiology, heart rate and HRV have been treated descriptively,

and, through the use of stimulation and blockade paradigms,

these variables have been used to infer the inﬂuence of heart rate

on global neural regulation systems (i.e., vagal or sympathetic).

However, the polyvagal perspective shifts the metaphor of

inquiry by emphasizing neurophysiological mechanisms and

adaptive functions. For example, the polyvagal perspective

emphasizes the involvement of peripheral physiological activity

in a ‘‘system,’’ how this ‘‘system’’ maintains bidirectional

communication between central (e.g., brain) and peripheral (e.g.,

autonomic, behavioral) components, and how the adaptive

functions of this system relate to various phylogenetic stages

(e.g., Jackson, 1958). The polyvagal perspective attempts to

dispel ‘‘discipline’’ myths by questioning assumptions that do

not transcend levels of inquiry.

Four global levels of inquiry have been used in the

psychophysiology literature. First, heart rate parameters have

been used as either dependent or individual difference

variables, without acknowledging the role of speciﬁc peripheral

physiological mechanisms involved in the regulation of beat-to-

beat heart rate. By excluding knowledge of peripheral

physiology, explanations focus on statistical issues (e.g.,

reliability) and sensitivity to the experimental manipulation.

Second, heart rate parameters have been used as a peripheral

physiological response, without acknowledging the role of

speciﬁc central structures and neural pathways and feedback

circuits. By excluding this knowledge, constructs such as

cardiac vagal tone emerge without an attribution to the vagal

efferent pathways, the source nuclei, the inﬂuence of afferent

feedback, and the profound effects that central circuits have on

the selective modulation of speciﬁc vagal pathways to the heart.

Third, heart rate parameters have been studied from a

neurophysiological perspective. Fourth, heart rate response

parameters have, as in the polyvagal theory, been studied from a

neurobiological perspective that includes an understanding of

phylogenetic and embryological contributions. Incorporation

of phylogenetic information allows an understanding of the

adaptive nature of the heart rate response.

The polyvagal theory provides a perspective that encourages

an appreciation of both underlying neurophysiological pro-

cesses and neuroanatomical structures that express both

developmental and adaptive phylogenetic transitions. The

polyvagal perspective builds on the underlying neural

structures, mechanisms, and processes related to adaptive

autonomic reactions. This perspective guides research toward

testing speciﬁc hypotheses, searching for speciﬁc neural

mechanisms and mediators, asking fundamental questions

regarding adaptive features of speciﬁc responses, and

formulating speciﬁcations for methods and techniques. For

example, the polyvagal perspective could address several

contemporary issues including: (1) how RSA is quantiﬁed; (2)

S.W. Porges / Biological Psychology 74 (2007) 116–143 127

how HRV is decomposed and the components interpreted; and

(3) how the mechanisms mediating HRV are related to the

expression of emotion and the facilitation of social engagement

(e.g., social engagement system).

4.2. Heart rate and HRV: a psychological perspective

As psychophysiology grew as a discipline, it inﬂuenced

several areas of psychology (e.g., developmental, clinical,

social, health). Researchers in these subdisciplines embraced

the use of physiological variables as an index or window into

the psychological processes they studied (e.g., stress, attention,

mental effort). Physiological variables were assumed to be

objective measures of psychological processes, especially

when the processes were difﬁcult to infer from observable

behaviors. For example, in the late 1960s, heart rate

deceleration was demonstrated to parallel the changes in

stimulus parameters theoretically assumed to elicit an orienting

response (Graham and Clifton, 1966). Heart rate deceleration,

as a quantiﬁable physiological response, was rapidly trans-

formed into a psychological construct, cardiac orienting (e.g.,

Jackson et al., 1971). As a construct, cardiac orienting

emphasized the covariation between a psychological process

(i.e., orienting) and a physiological response (i.e., heart rate

deceleration). However, cardiac orienting implied not only that

when an individual oriented heart rate decelerated, but also that

when heart rate decelerated orienting occurred. This logic

illustrates how, without an understanding of the neural

regulation of the heart, a false assumption regarding a

bidirectional covariation between psychological and physio-

logical processes may be made.

The misunderstanding starts with the application of an

experimental design and statistics to test hypotheses related to

covariation (i.e., regression). Using this strategy, the literature

illustrates a strong covariance between the occurrence of

orienting and heart rate deceleration. However, the statistical

model employed in the experimental design had an implicit

directionality and, while focusing on the link from orienting to

heart rate deceleration, did not test adequately whether there

was a strong link from heart rate decelerations to orienting. The

model neglects the possibility that the heart rate decelerates

during conditions that are not related to ‘‘orienting.’’ However,

an understanding of neural regulation of the heart would

identify several neural mechanisms that produce rapid heart

rate decelerations (such as heart rate reactions to movement,

intention to move, posture shifts, breaths, and numerous well-

documented vagal reﬂexes) that occur independently from the

psychological process of orienting. Thus, a correlation between

heart rate deceleration and orienting could approach zero when

starting with the data domain of heart rate decelerations, or

approach unity when starting with the data domain of orienting

behaviors elicited by stimuli in the laboratory.

An extreme example of the successful acceptance of heart

rate in psychological paradigms is found in research in which

heart rate is treated as an observable behavior similar to the

coding of behavior in videos. In this example, coders transcribe

heart rate values from digital displays when testing infant

responses to various stimuli (e.g., Blass and Watt, 1999). These

quantiﬁcation procedures follow the rules used to code

observable behavior. These measures of heart rate, similar to

the coding of behavioral data, have high inter-rater reliability.

However, this strategy does not question the accuracy of the

heart rate displayed on the monitor or the precision of the R-

wave detection. Nor does it question the embedded algorithm

found in the clinical device that may display a running average

and dampen abrupt changes in heart rate. From a dependent

variable perspective, the strategy focuses not on mechanism,

but solely on reliability of the observer and sensitivity of the

operationally deﬁned variable to the experimental manipula-

tion. Research that treated physiology as a behavior dominated

the early history of psychophysiology and related areas that

have applied physiological variables as ‘‘correlates’’ or

indicators of psychological processes or psychiatric conditions.

Unfortunately, a lack of knowledge in physiology, neurophy-

siology, phylogeny, and adaptive function has great impact on

the questions, paradigms, methods, and interpretations avail-

able in psychophysiology.

In autonomic conditioning paradigms, heart rate measures

have been treated similar to observable behaviors. Although

these studies are characterized by careful experimental

procedures, there have been major failures. Some of these

failures may be attributed to a misunderstanding of the neural

mechanisms mediating the responses. In some cases, the failure

might have been due to the experimental manipulations

interacting with the neural regulation of the autonomic nervous

system and confounding the ability to quantify the variables

being studied.

In the late 1960s, Miller (see Miller, 1978 for review) and

others attempted to extend the domain of instrumental learning

to the autonomic nervous system. These studies provide an

important example of this hypothetical problem. By the early

1960s, there were reliable reports of classical conditioning of

heart rate in dogs (Black and Lang, 1964; Smith, 1967). In these

studies, to insure that skeletal muscles did not confound or drive

the heart rate responses, the dogs were completely paralyzed by

curare. Consistent with their colleagues, who studied classical

conditioning and were concerned that muscular activity might

mediate visceral responses, Miller and others conducted

experiments with rats paralyzed by curare and artiﬁcially

ventilated. The initial studies demonstrated operant condition-

ing of heart rate and other autonomic variables. Miller (1978)

stated that ‘‘these experiments were conﬁrmed by results in

three other laboratories, but later the results of apparently

similar experiments progressively declined until it became

impossible to repeat them in spite of extensive efforts in the

author’s laboratory and elsewhere.’’ The ‘‘loss’’ of this

phenomenon perplexed the psychophysiological community

and the researchers tried to ﬁnd an explanation (for details, see

Roberts, 1978). Experimental procedures were carefully

manipulated by controlling for movement and respiration.

Were the data from the early studies spurious? Were the studies

testing a non-existent phenomenon? Were the protocols

inappropriate to study voluntary changes in heart rate and

other visceral processes? The observed inability to reliably

S.W. Porges / Biological Psychology 74 (2007) 116–143128

demonstrate instrumental heart rate conditioning in a curarized

mammal is obvious, if the paradigm is deconstructed from the

polyvagal perspective.

From a behavioral perspective, the ﬁrst concern is to remove

the potential inﬂuence of skeletal motor activity on autonomic

reactivity. Curare is effective in blocking the nicotinic receptors

on the post-synaptic membrane of the neuromuscular junction

and results in paralysis. Thus, the scientists studying classical

and instrumental conditioning were effectively blocking the

potential confounding inﬂuence of skeletal motor activity on

the putative conditioned heart rate responses. This worked ﬁne

with the classical conditioning paradigms, but not with the

instrumental conditioning paradigms.

From the polyvagal perspective, the ﬁrst concern is to

identify the neural mechanisms of the conditioned heart rate

response and to understand the adaptive features of the

response. Based on the classical conditioning literature, heart

rate deceleration is reliably observed even during states of

curare-induced paralysis. This observation enables us to

identify the unmyelinated vagus, with its source nucleus in

the dorsal motor nucleus of the vagus, as the neural mechanism

mediating the classical conditioned heart rate response. This

conclusion is based on the selective effects of curare on

nicotinic receptors. Not only does curare block nicotinic

receptors at the post synaptic membrane of the neuromuscular

junction to produce paralysis, but it also blocks nicotinic

preganglionic receptors in the sympathetic nervous system and

in the sino-atrial node communicating with the myelinated

vagus originating in the nucleus ambiguus. Thus, functionally,

curare removes the primary modes of rapid neural regulation of

heart rate, leaving only neural mechanisms dependent on

muscarinic receptors (e.g., the unmyelinated vagus to the

heart). This explains the inability to instrumentally condition

heart rate in a curare preparation, while preserving the neural

mechanism mediating classically conditioned responses that

are mediated via muscarinic cholinergic receptors (e.g., heart

rate decelerations and sudomotor activity). Roberts (1978)

provides additional plausible explanations in a detailed review

of the ‘‘fragility’’ of conditioning under curare.

4.3. Heart rate and HRV: a physiological perspective

The study of beat-to-beat heart rate patterns as a peripheral

physiological response often involves the application of basic

physiological tools (i.e., surgery, stimulation, and pharmacol-

ogy manipulations) to determine neural function. For example,

neural blockades can be used to determine whether vagal or

sympathetic pathways regulate the heart rate response to a

speciﬁc stimulus. Beta-blockers (e.g., propranolol or atenolol)

can be used to determine sympathetic inﬂuences, and blocking

the function of acetylcholine muscarinic receptors with

atropine can be used to determine vagal inﬂuences.

Hypothetically, pharmacological blockade would be an

effective method to evaluate cardiac vagal tone, if two

restrictions were met: (1) the variable being measured is

determined by vagal efferent action on the heart, and (2) the

vagal efferent action on the heart is mediated by a

homogeneous neural pathway regulated by a single neuro-

transmitter via a common receptor. Under these constraints, a

blockade would dampen or block vagal inﬂuences on the heart

without inﬂuencing other structures or neural circuits.

Unfortunately, such a restricted model seldom occurs in

dynamically regulated neurophysiological systems. The vagal

inﬂuences on the heart via myelinated and unmyelinated vagi

constitute two efferent limbs of a complex feedback circuit

regulating the heart. Not only are the two vagal pathways

originating in different brainstem areas, but the vagal efferent

inﬂuences on the heart are conveyed through both myelinated

ﬁbers with selective inﬂuence on nicotinic preganglionic

receptors, and unmyelinated ﬁbers with selective inﬂuence on

muscarinic preganglionic receptors. Since all vagal efferent

ﬁbers inﬂuence post-ganglionic muscarinic receptors, atropine

is an effective blockade of total vagal efferent inﬂuence from

both vagal pathways.

Standard methods of blockade or surgery, which have been

used to identify vagal mechanisms mediating heart rate, cannot

distinguish between the speciﬁc vagal pathways originating in

either the nucleus ambiguus or the dorsal motor nucleus. Since

vagal regulation of the heart is part of a complex feedback

system, blockade could inﬂuence other features of the system

regulating the heart. For example, a change in heart rate might,

via afferent feedback, inﬂuence the heart directly, via neural

mechanisms, or indirectly, through changes in vasomotor tone

or blood pressure. Similarly, sympathetic blockade could

inﬂuence vagal pathways indirectly by changing the state of the

heart and altering afferent feedback to the central structures

regulating cardiac vagal tone. Attempts to create total neural

blockade by using more than one drug might, due to complex

pharmacokinetics, result in interactions that cannot be

explained as an additive model. In addition, partial blockade

manipulations with low doses are not reliable manipulations of

neural tone, since with low doses there are large individual

differences in sensitivity to the traditional blockade drugs.

Current research in the neurophysiology of cardiovascular

regulation is generating new knowledge regarding the

selectivity and speciﬁcity of vagal pathways and pre- and

post-ganglionic muscarinic and nicotinic receptors (e.g., Wang

et al., 1995; Neff et al., 2003). Thus, our understanding of the

neural mechanisms mediating heart rate patterns derived via old

methods, even the trusted blockade strategy, need to be

cautiously evaluated.

4.4. Cardiac vagal tone: the search for a criterion variable

Physiological strategies may result in circular reasoning

when deﬁning a criterion variable. For example, to validate

RSA, as an index of cardiac vagal tone, the researcher might

demonstrate that RSA is depressed by blocking acetylcholine

(i.e., the neurotransmitter of the efferent vagal pathways to the

heart) transmission with atropine (e.g., Dellinger et al., 1987;

Porges et al., 1982). Or, since basal heart rate is primarily under

vagal control, the researcher might use the change in heart rate

in response to atropine or reversibly cooling the vagus as a

criterion measure and correlate this change with RSA (e.g.,

S.W. Porges / Biological Psychology 74 (2007) 116–143 129

Katona and Jih, 1975). Additional examples exist in which

there are attempts to reﬁne the heart rate response as a criterion

variable to contrast with RSA. For example, beta-blockers are

administered to remove sympathetic inﬂuences from the heart

rate response (Grossman et al., 1990a). In other studies, minute-

to-minute changes in heart rate over a 24 h period, assumed to

be related to physical activity, have been used as an index of

cardiac vagal tone (Grossman et al., 2004).

What is the criterion variable for cardiac vagal tone? A

major problem with concretizing and validating a measure of

cardiac vagal tone is the need to identify and to agree on a

criterion variable. From a physiological perspective, a variable

that is extremely sensitive to manipulations known to attenuate

or block vagal efferent activity would qualify. Historically,

heart rate in response to atropine has been the most commonly

used surrogate variable for cardiac vagal tone. Since all vagal

post-ganglionic receptors are muscarinic, high doses of

atropine effectively disrupt all vagal inﬂuences to the heart.

This strategy assumes that the vagus acts as a unitary pathway,

the vagal efferent activity can be effectively blocked by

atropine, and that the sum of the vagal activity is meaningful

and can be accurately assessed by the change in heart rate.

Atropine blockade as a test for vagal inﬂuence became part

of the physiologist’s tool box long before an in depth

understanding of the function and structure of the two vagal

pathways were acknowledged and studied. In our laboratory,

although we acknowledge the limitations of the blockade

methodology, we have used atropine blockade to emphasize the

sensitivity of RSA to traditional methods for evaluating vagal

inﬂuences. We have used this blockade approach with several

mammalian species to conﬁrm that RSA was mediated via the

vagus (see Porges et al., 1982).

Other than correlations, how can the various methods that

quantify RSA or other components of HRV be contrasted?

Without an accepted criterion variable, how can an index of

cardiac vagal tone be established? Consistent with the APA

Task Force on Statistical Inference (1999), relative size of effect

(i.e., Cohen’s d) in response to blockade could be used to

contrast the sensitivity of RSA and heart rate and to determine

which variable is the better surrogate variable for cardiac vagal

tone. This procedure provides a metric to contrast the

sensitivity of different variables to blockade. The strategy

provides a platform to empirically describe the sensitivity of

several variables to vagal blockade and to determine which

variable (e.g., RSA, global measures of HRV, or heart rate) is

most sensitive to atropine or inﬂuenced by beta-blockade.

Subsequent research can evaluate whether measures that have a

validated neurophysiological mechanism are more or less

sensitive to speciﬁc psychological processes and behaviors.

This strategy, by identifying neural mechanisms, provides an

opportunity to describe the linkage between a neurophysiolo-

gical mechanism and the psychophysiological relation being

studied.

Several years ago in our laboratory, HRV was monitored in

college-aged male subjects during an atropine dose–response

experiment (Dellinger et al., 1987). A re-analysis of the

available data allows us to contrast the effect size of heart

period, RSA, and a slower ‘‘LF’’ rhythm (0.06–0.10 Hz). As

illustrated in Fig. 3, all variables exhibited strong signiﬁcant

dose-dependent attenuations due to atropine. In response to

increasing doses of atropine, heart period became shorter and

both measures of HRV substantially decreased and approached

measurement error. To contrast the effect size of the variables,

Cohen’s d(Cohen, 1988) was calculated to provide a

standardized estimate of effect size for all variables. Cohen’s

dis calculated by dividing the mean of the difference scores

(e.g., change from a placebo dose to each dose of atropine) by

the standard deviation of the difference scores. Thus, a d=1

would be equivalent of a mean difference of one standard

deviation in response to the treatment, independent of the unit

of measurement and sample size. As a general guide Cohen

proposes interpreting d= .2 as a small effect, d=.5 as a

medium effect, and d= .8 as a large effect.

Most interesting is that the two commonly extracted periodic

processes from the heart rate spectrum, RSA and LF, were

extremely sensitive to atropine with effect sizes of approxi-

mately 5.0, which is twice the size of effect for heart period.

Note that LF has been assumed in the literature to be sensitive to

sympathetic inﬂuences and is frequently described as

representing sympathovagal balance (for review, see Eckberg,

1997). If the size of effect in response to atropine were used to

evaluate cardiac vagal tone, then one could empirically argue

that both RSA and LF are more sensitive indices of cardiac

vagal tone than heart period. These examples illustrate an

application of the physiologist’s toolbox in determining

plausible surrogate variables for cardiac vagal tone.

In an unpublished study, partial and full neural blockades

were administered to older (27–70 years of age) human

participants. Consistent with the previous data, the effect size of

atropine was greater for the two heart rate rhythms than for

heart period. When atropine was given as the ﬁrst blockade,

RSA was totally abolished. The effect size of the immediate

administration of atropine was above 2.0 for both RSA and LF

and about 1.5 for heart period. In contrast, propranolol (a beta-

blocker), although signiﬁcantly inﬂuencing heart period, had no

inﬂuence on either RSA or LF. However, when propranolol was

S.W. Porges / Biological Psychology 74 (2007) 116–143130

Fig. 3. Atropine sulfate dose–response curve. HP (heart period in ms), RSA

(respiratory sinus arrhythmia amplitude in ln ms

) and LF(low frequency

amplitude in ln ms

). Atropine dose is per 75 kg of body weight. A placebo

was used for the 0 mg dose.

administered, while the effects of atropine were still active,

there was an increase in RSA and heart period to approximately

the mid-point between atropine and baseline. The effect of full

blockade on heart rate is predictable and may be explained as

the sum of two functional effects, one increasing heart rate (i.e.,

vagal blockade) and one decreasing heart rate (i.e., sympathetic

blockade). However, the effect on RSA is puzzling. How can a

sympathetic blockade, which has no inﬂuence on RSA when

given alone, increase RSA when the participant has been

‘‘primed’’ with atropine? Similarly, the effect of atropine was

attenuated to this ‘‘midpoint,’’ if atropine was administered

while the effects of propranolol were still active. Even more

perplexing, LF, which similar to RSA was greatly attenuated

with atropine and unaffected by propranolol when given

separately, did not express this ‘‘midpoint’’ phenomenon when

propranolol was given simultaneously with atropine. We

recently completed an autonomic blockade study with prairie

voles with similar manipulations (Grippo et al., in press). In the

prairie vole, RSA was selectively reduced by atropine and not

inﬂuenced by atenolol (a beta-blocker). The effect size of

atropine on RSA was 2.25 compared to 0.33 for heart period.

When atenolol and atropine were simultaneously administered,

similar to the dual blockade study with humans described

above, both heart period and RSA were at approximately 50%

of baseline level. Although beta-blockade appears to diminish

the effect of atropine on RSA, it does not imply that there is a

sympathetic component to RSA. This effect appears to reﬂect a

complex interaction involving pharmacokinetics and receptors,

since beta-blockade by itself had not effect on RSA.

Methods that use change in heart rate in response to

blockade as the criterion for quantifying neural regulation are

vulnerable to the well-documented neural interactions on heart

rate. If we assume that vagal inﬂuences from the nucleus

ambiguus have an ‘‘inhibitory’’ effect on sympathetic activity,

then removal of the vagal inﬂuence to the heart would

simultaneously disinhibit sympathetic activity, thus, explaining

why changes in vagal efferent activity have a larger impact on

heart rate when sympathetic activity is high. However, since the

sympathetic nervous system appears to have little or no direct

inﬂuence on RSA and LF, measurement of RSA and/or LF may

be more linearly related to vagal efferent activity and

insensitive to the interaction due to variations in sympathetic

tone observed in heart rate.

Although a powerful tool in determining global neural

inﬂuences, it could be argued that the physiologist’s toolbox is

limited because it cannot distinguish the unique contributions

of each of the two vagal pathways. A neurophysiological

strategy would conﬁrm that although the two vagal pathways

are mediated by acetylcholine and can be blocked with

atropine, only the vagal ﬁbers originating in the nucleus

ambiguus have a respiratory rhythm directly inﬂuencing

preganglionic nicotinic receptors. Rather than emphasizing

this difference between the two vagal pathways, the physiol-

ogist’s toolbox supports a discipline myth that confuses the

relation between RSA and neurophysiological mechanisms by

relying on a surrogate criterion variable, such as change in heart

rate in response to atropine (e.g., Katona and Jih, 1975), or heart

rate changes associated with movement (Grossman et al.,

2004), or even heart rate after a partial beta-blockade

(Grossman et al., 1990a), that functionally sum across all

vagal efferent inﬂuences to the heart. These techniques are

theoretically and functionally removed from the unique

features (e.g., a respiratory rhythm) and functions (e.g.,

maintaining an appropriate diffusion gradient for oxygen) of

the neural pathways originating in the nucleus ambiguus

(Hayano et al., 1996; Taylor et al., 1999).

Although there is general acceptance that RSA is mediated

through the vagus, there is debate and confusion in the literature

about whether the amplitude of RSA is a legitimate index of

cardiac vagal tone. Arguments for this relation are based on the

ﬁndings that RSA is virtually abolished with total vagal

blockade and that RSA exhibits a dose response curve to

atropine. Moreover, as illustrated in Fig. 4, the effect sizes of

atropine dose on RSA are greater than on heart period.

Although these ﬁndings suggest that RSA is more sensitive to

vagal blockade than heart period, it has been argued that RSA

must be corrected for breathing parameters to be an accurate

index of cardiac vagal tone (e.g., Grossman et al., 1990a).

During the past few years, there has been a better

understanding of vagal mechanisms and the neurophysiology

of RSA. No longer is RSA deﬁned solely by its covariation with

peripheral respiratory activity. Neurophysiologists have estab-

lished that RSA is the functional output of cardioinhibitory vagal

efferent ﬁbers that originate in the nucleus ambiguus (for review,

see Porges, 1995; Neff et al., 2003), and that these pathways have

a respiratory rhythm, are myelinated B-ﬁbers, respond with short

latencies, and function through nicotinic preganglionic receptors

(Mendelowitz, 1996; Mendelowitz and Kunze, 1991). These

vagal efferent pathways that originate in the nucleus ambiguus

are inherently silent and require afferent feedback via the sensory

vagus (i.e., tractus solitarius) and inputs from central structures

(Neff et al., 1998a,b; Wang et al., 2001) to communicate with the

sino-atrial node. Thus, the concept of a constant ‘‘central’’ vagal

tone, independent of peripheral feedback and central modulation,

is not neurophysiologically valid. Other cardioinhibitory ﬁbers

originate in the dorsal motor nucleus of the vagus. These

pathways are unmyelinated C-ﬁbers that respond with longer

latencies and function through the muscarinic preganglionic

receptors (Cheng and Powley, 2000). B-ﬁbers have a faster

S.W. Porges / Biological Psychology 74 (2007) 116–143 131

Fig. 4. Atropine sulfate dose–response curve: size of effect. Cohen’s dis

calculated for the effect size for each variable contrasting placebo condition

(0 mg) with each of the four doses.

conduction velocity (3–15 m/s) than C-ﬁbers (1–3 m/s). Stimu-

lation of both vagal pathways produces bradycardia, although

stimulation of B-ﬁbers produces a shorter latency and larger

magnitude heart rate response. Post-ganglionic vagal efferent

pathways from both vagal sources function through muscarinic

receptors. Thus, atropine is effective in blocking all sources of

vagal activity, but does not allow the extraction of an accurate

index of the function of either nucleus.

With this knowledge, a plausible model can be structured to

relate RSA to cardiac vagal tone. Operationally, cardiac vagal

tone (CVT) would be equivalent to the sum of the inﬂuences of

the cardioinhibitory pathways originating in both the nucleus

ambiguus (NA) and the dorsal motor nucleus of the vagus

(DMX) or CVT = NA + DMX. Atropine blocks both vagal

sources, which results in the monotonic relation between

atropine dose and RSA amplitude that is observed (see Fig. 3).

However, although RSA appears to be a sensitive index of vagal

pathways originating in the nucleus ambiguus, there is no

apparent index of the other limb of this additive model (i.e., the

inﬂuence of vagal pathways originating in DMX on the heart).

4.5. The selection of measurement parameters: an implicit

theory

Although less interested in physiological and neurophysio-

logical mechanisms, psychophysiologists have set the standard

for methodology by advocating greater precision and accuracy

in heart beat detection and expressing a concern for methods to

deal with transitory disruptions in the beat-to-beat pattern due

to arrhythmia and artifact (see Porges and Byrne, 1992). In

contrast, publications in physiology often rely on global

measures of HRV (e.g., range, standard deviation), with less

precision (e.g., use of slow sampling rates for the ECG or use of

pulse waves to detect heart beat changes), and without setting a

standard for editing transitory disruptions in the beat-to-beat

pattern due to either arrhythmia or recording artifact.

Faulty R-wave detection or the presence of an arrhythmia

will inﬂuence the timing of sequential R–R intervals with a

resultant apparent rapid change in heart rate. The technologies

used to describe RSA and other measures of HRVare especially

vulnerable to spurious rapid changes in heart rate that will, by

default, be attributed to the higher frequencies in the heart rate

spectrum. Even when using the time domain algorithms (e.g.,

overall variance, variance in a frequency band, or breath-to-

breath changes) the estimate of RSA can be confounded by

faulty R-wave detections (e.g., Byrne and Porges, 1993). Thus,

the quantiﬁcation of RSA, regardless of the method, is

extremely sensitive to artifact.

Since arrhythmias are physiological processes, why should

they be edited? How would a faulty detection be identiﬁed and

how should it be edited? If arrhythmias are true physiological

processes, why should they be ‘‘edited’’ or adjusted in the time

series of R–R intervals? Or, more speciﬁcally, which types of

arrhythmias would confound the quantiﬁcation of periodic

rhythms in heart rate? The polyvagal perspective justiﬁes speciﬁc

solutions to speciﬁc problems of editing artifact and arrhythmias.

From a neurophysiological perspective, RSA is linked to the

vagal efferent inﬂuence on the sino-atrial node. RSA is an atrial

rhythm. Thus, ventricular arrhythmias, such as ectopic

ventricular complexes followed by a fully compensatory pause,

would inﬂate the quantiﬁcation of RSA by contributing

additional variance due to ventricular activity, independent of

the vagal modulation of the sino-atrial node. Therefore, these

arrhythmias should be edited by summing the atypical short and

compensatory long intervals. The mean of these two intervals

will closely approximate the expected atrial rhythm and

effectively remove the confounding ‘‘ventricular’’ source of

variance. Not editing this type of arrhythmia will inﬂate the

estimate of RSA, since the rate of heart rate changebetween these

two beats will, via the statistical decomposition of the time series,

attribute additional variance to a frequency band associated with

breathing. This will occur regardless of the quantiﬁcation

strategy, including time domain methods (e.g., band-pass),

frequency domain methods (e.g., spectral), and global descrip-

tive statistics (e.g., peak-valley, range, variance).

Although movement artifact needs to be edited, the

identiﬁcation of artifact can be difﬁcult. There are several

critical issues in developing a strategy to edit artifact. From a

‘‘dependent’’ variable model, there is no information to guide

the researcher. From a physiological model, we know the range

of heart rate in the species. However, from a neurophysiological

model, we need to know the range of heart rate change that may

occur between two adjacent beats and how this range may vary

as a function of neural inﬂuences. When a species has low

amplitude RSA, rapid heart-to-beat changes are minimal and

plotting the data can easily identify abrupt changes. Detections

of artifact can be identiﬁed with simple algorithms that ﬂag

sequential beats that change by a large percent. For example,

the beat-to-beat variation in humans usually ﬂuctuates within

the range of 75–135%. Missed or ‘‘double’’ detections can be

corrected with algorithms based on integer arithmetic (i.e.,

adding or dividing the intervals of two sequential data points).

However, difﬁculties in this decision process occur when the

species tested have high amplitude RSA that can be expressed

as beat-to-beat changes in the range of 50–200%. For example,

adolescent humans, prairie voles, and various species of dogs

have very high amplitude RSA. The prairie vole provides an

interesting example of this problem. The prairie vole weighs

about 50 g and, when physically active, has a heart rate similar

to a mouse (see Grippo et al., in press). However, when

quiescent with a partner, the heart rate is slower than a 400 g rat.

When vole beat-to-beat heart rate is plotted, at times the heart

period will rhythmically and rapidly transition between 100 and

200 ms. To conﬁrm that these rapid large changes were not due

to faulty R-wave detections, we developed software to

superimpose the ECG on the time series of R–R intervals.

The software enables the researchers to identify and correct

faulty R-wave detections. Without this software, applying

general rules across species (e.g., using parameters from

humans, rats, or mice) would have attenuated the ‘‘true’’ RSA.

This attenuation of the true amplitude of RSA would occur even

if reliable rules of quantiﬁcation were applied. Thus, before

a strategy for artifact rejection and adjustment can be

implemented, an understanding of the beat-to-beat pattern

S.W. Porges / Biological Psychology 74 (2007) 116–143132

for the participants needs to be known. The researcher needs to

know the expected value of heart rate and an estimate of the

distribution of change scores between adjacent beats.

The treatment of heart rate or RSA as a dependent variable

similar to behavior requires only an atheoretical empirical

perspective. Although this strategy may produce reliable

ﬁndings, it will not lead to the development and application of

methods necessary to investigate the mechanisms mediating the

responses. For several years, it was assumed that 8 ms was

sufﬁcient to quantify beat-to-beat heart rate, since many

commercial clinical monitors in hospitals had this precision.

Similar arguments were made with of pulse measures (e.g.,

derived via plethysmography, phonography, or ultrasonogra-

phy) as a surrogate metric for the ECG, such that these

measures were sufﬁcient for accurate calculation of heart rate in

clinical settings. This, of course, was a truthful statement in

estimating average heart rate over a few seconds. However, it

imposed a fuzzy lens when researchers attempted to study beat-

to-beat patterns and applied statistical methods to decompose

HRV into periodic components. Although poor precision in the

measurement of heart rate provided stable average values, it

impeded the opportunity to study small amplitude periodic

components in the HRV.

Although seldom described in manuscripts, the method of

beat-detection provides another example of how the precision

and accuracy of quantifying R–R intervals may inﬂuence the

data stream sufﬁciently to impede the ability to investigate

neural mechanisms. Reviewers seldom query authors about the

algorithms that they use to detect R-waves. Nor do they

distinguish among the major sources of error variance in

the quantiﬁcation of heart rate: timing precision (i.e., sampling

rate necessary to quantify R–R intervals), accuracy of the R-

wave detection (i.e., how close to the peak of the R-wave is the

detection made), treatment of faulty detections, and inﬂuence

of arrhythmias.

Since cardiovascular psychophysiology is primarily con-

ducted with commercial software and hardware, the researcher

is a consumer who is seldom involved in the development and

standardization of the parameters of R-wave detection and R–R

quantiﬁcation. Of course, precision is easily understood, and

most scientists argue for a higher precision and follow

guidelines of quantifying ECG at 500 Hz or 1 KHz. However,

the information on R-wave detection is seldom provided. Both

the amplitude of R-waves and the baseline ECG pattern

inﬂuence detection of R-waves, and these parameters are not

stable. To facilitate R-wave detection, electrode placement may

be manipulated to maximize the R-waves relative to other

components, and hardware ﬁlters can be used to stabilize the

baseline ECG signal. Although ﬁlters stabilize the base level of

ECG and provide a more easily observable R-wave, ﬁlters may

distort the shape of the R-wave and may shift the temporal point

of the peak by removing some of the higher frequency

components that contribute to the R-wave.

In the early days of psychophysiology, voltage level

detectors were used to drive tachometers that provided

information on heart rate. To maximize the detection of R-

waves, the level was often conservatively set to trigger on most

beats. Since level was used and the amplitude of the R-wave

varied, the part of the R-wave that triggered the level detector

varied across beats. This ‘‘error’’ variance was reduced with the

implementation of slope detectors that, via hardware or

software, attempted to identify the inﬂection point of the R-

wave. However, the accuracy of the slope detection is

dependent on the algorithm and, in part, on the sampling rate.

The issue of precision and accuracy is imbedded in the

polyvagal perspective. The polyvagal perspective motivates

the researcher to study both the functional output and the

peripheral and central mechanisms mediating the output of

the two vagal systems. The polyvagal perspective directs the

researcher to apply the best available technologies to measure

low amplitude periodic processes in the beat-to-beat pattern.

Thus, this perspective enables the researcher to have a vested

interest in applying the most accurate and precise methods to

measure R–R intervals and to search for underlying

mechanisms. These issues become more problematic when

organisms with low amplitude RSA are tested, such as

anesthetized mammals, preterm infants, and other high-risk

clinical populations.

Since the polyvagal perspective is vested in identifying

underlying mechanisms, it encourages the researcher to

question even the appropriateness of the R–R interval as the

metric for the study of vagal inﬂuences on heart rate. This

question arises through the convergence of several neurophy-

siological and physiological phenomena. First, cardioinhibitory

vagal efferent ﬁbers that originate in the nucleus ambiguus have

a respiratory rhythm. Second, the vagal ﬁbers synapse on the

sino-atrial node. Third, the sino-atrial node is the heart’s

pacemaker and initiates the start of a heartbeat. Fourth, the

heartbeat is initiated when depolarization spreads from the

sino-atrial node through the atria and is manifested in the ECG

as a p-wave. Fifth, the ‘‘rhythmic’’ cardioinhibitory vagal

efferents functionally produce RSA in the heart rate pattern by

inhibiting and releasing from inhibition the sino-atrial node.

Although the expected value of R–R intervals is equivalent

to the expected value of p–p intervals, the sequential beat-to-

beat pattern could vary. Thus, from the polyvagal perspective,

the time course of p–p intervals, hypothetically, would be more

sensitive than R–R intervals to the cardioinhibitory inﬂuence

originating the nucleus ambiguus. Unfortunately, due to the low

amplitude of the p-wave relative to the R-wave, current

technology (i.e., ECG ampliﬁers, software algorithms) is

limited, especially when the signal is being monitored through

surface electrodes that have been placed to minimize movement

artifact in the ECG signal. Animal models, using mammalian

species with high cardiac vagal tone, might provide an

opportunity to reﬁne these technologies. However, before

resources can be directed towards developing new technolo-

gies, the research community must have an in depth under-

standing of neural inﬂuences on the sino-atrial node.

4.6. Statistics may be misleading

Statistical techniques may mislead scientists to overestimate

relationships describing the speciﬁcity between physiological

S.W. Porges / Biological Psychology 74 (2007) 116–143 133

responses and psychological processes. Interpretations of

strong relations between physiological variables and psycho-

logical processes are dependent on observation constraints and

an implicit directionality of the relationship. Strong correla-

tions approaching unity can be observed between physiological

variables and psychological processes in laboratory paradigms

focusing on the psychophysiology of affect and cognition.

Although a physiological response with predictable features

may always occur during a speciﬁc psychological process, this

does not provide information regarding the possibility that the

same physiological response may occur independent of the

psychological process. Scientists often use these strong ﬁndings

of physiological-behavioral parallels to argue for the identi-

ﬁcation of a speciﬁc physiological, neural, or brain signature

for a psychological process. This has occurred with cardiac

orienting (see above), in which heart rate deceleration was used

inappropriately as an interchangeable construct with orienting

and attention. Similar issues are seen with various ERP

components that have been assumed only to occur during

speciﬁc cognitive tasks. Most recently, fMRI imaging

procedures have identiﬁed areas of the brain that are activated

during affective states. These brain areas are often assumed to

function solely as a source of affect without an understanding of

the interconnectiveness of neural circuits and their potential

functions. Other physiological variables that have been

embraced by psychology, such as cortisol and oxytocin, have

been used in the literature as physiological indices of

psychological processes. Increases or high levels of salivary

cortisol frequently have been used interchangeably with the

construct of stress. This assumed isomorphism neglects the

important adaptive functions of cortisol in converting

norepinephrine to epinephrine, in breaking down lactate, and

in regulating surfactant (e.g., see Porges, 2001b). Similarly, the

important ﬁndings linking positive social experiences to

oxytocin are often discussed independent of the important

role that oxytocin has peripherally in regulating autonomic

state (i.e., during nursing and partuition) and centrally in

modulating the outﬂow of vagal efferent activity from the

dorsal motor nucleus of the vagus (see Porges, 2001a).

A physiological state that covaries with a psychological

process will generally be observed in settings independent of

the context in which the psychological process occurs. This is,

of course, the same problem that may be observed with

measures of brain function, since the nervous system is not

solely subservient to speciﬁc psychological processes, whether

or not they require conscious awareness. Thus, physiological

‘‘correlates’’ of psychological processes are seldom unique and

speciﬁc indicators of that process, although psychophysiology

has not vested resources in investigating the covariation of

psychological processes with physiological processes when

‘‘selecting’’ from a time series of physiological activity across

contexts, demands, and behavioral states. Unfortunately, the

assumption that there are cognitive and affective signatures in

the brain and nervous system and that the search for these

signatures constitutes valid scientiﬁc inquiry, promotes an

intellectual drift in our science towards the treatment of

physiological or neurophysiological responses as speciﬁc (as

contrasted with general states that promote a range of behaviors

and psychological processes) attributes of the cognitive or

affective process.

Extrapolations relating psychological processes to physio-

logical variables are often overstated, because most neurophy-

siological and physiological systems reﬂect similar features

during other contexts when the psychological process of

interest is not occurring. The nervous system is constantly at

‘‘work’’ and instances of physiological-behavioral covariation

do not necessarily mean that the physiological parameters can

be used to index speciﬁc psychological processes. The

polyvagal perspective, which incorporates an emphasis on

both neurophysiological mechanisms and adaptive functions,

addresses this problem by proposing the plausibility that

speciﬁc physiological states support or facilitate general

domains of behavior such as social engagement behaviors or

the defensive strategies of ﬁght, ﬂight, or freeze. Thus, although

the covariation between a physiological variable and a

psychological process clearly implicates an important relation-

ship, to better understand the neurobiology underlying speciﬁc

psychological processes, it is necessary to understand the

broader range of functions in which these neural systems are

involved.

Statistical techniques may mislead scientists to misinterpret

constructs such as cardiac vagal tone. Regression models (i.e.,

either correlation or analysis of variance) may be problematic

when attempts are made to validate the hypothesis that a

physiological variable is mediated by a speciﬁc neural

mechanism (i.e., cardiac vagal tone). Since these validation

studies generally apply the physiologist’s toolbox (consisting of

blockade, surgery, and electrical stimulation), post treatment

measures have a restricted range of individual differences

relative to pre-treatment measures. Often the studies evaluating

neural mechanisms are conducted while the organism is

anesthetized. Anesthetics often make it difﬁcult to study neural

regulation of the heart, since several anesthetics have direct

effects on vagal efferent tone to the heart.

Statistical techniques may mislead scientists to assume that

highly correlated methods are interchangeable. Methods of

quantifying RSA are not equivalent. Although statistics can be

used to demonstrate high inter-variable correlations, these high

correlations do not provide evidence of equivalence (e.g.,

Grossman et al., 1990b). If we return to questions of precision,

we can see how this may occur. If we have a dataset of measures

of RSA calculated with 1 ms precision and smooth these data to

a precision of 5 ms or even 10 ms, the correlation between the

two measures will be very strong and approach unity (see

Riniolo and Porges, 1997). Alternatively, we can reduce

precision by assigning subjects into a high and low RSA groups

and correlate group assignment with individual values. With the

dataset of 44 normal adults described in Denver et al. (in press),

the correlation was .83. Similarly with a dataset of 94 typically

developing preschool children, the correlation was .82. When

each sample was divided into quartiles, the quartile assignments

correlated .94 with the individual measurements of RSA. Since

both samples had a similar range of RSA, the correlations

were similar. Even with the restricted range of RSA observed in

S.W. Porges / Biological Psychology 74 (2007) 116–143134

these samples of healthy normal participants, the global

estimate of RSA associated with group assignment (i.e., median

split, quartile) was highly correlated with the individual scores.

If our correlations included clinical samples with disorders such

as hypertension, diabetes and depression, then the range of RSA

values would expand and the correlations would potentially

increase. Thus, even when the precision and accuracy of the

quantiﬁcation strategy is greatly reduced by smoothing across

individual differences, either by reducing sampling rate and

decreasing trigger accuracy or by assigning into global groups,

the correlations between the highly precise and accurate

methodology and the smoothed one will be very high. Thus,

methodologies can blur the range of individual differences (see

Riniolo and Porges, 1997) and coax investigators into assuming

equivalence of methods without testing whether there are

differences in sensitivity to experimental manipulations or

neural inﬂuences. Researchers must, therefore, be extremely

cautious of justiﬁcations for methods that focus on correlations

with other established techniques, because two highly

correlated methods might be differentially sensitive to

individual differences and to the underlying neurophysiological

mechanisms.

4.7. Decomposition of HRV: a polyvagal perspective

The publication of the international guidelines for the

quantiﬁcation of HRV (Task Force of the European Society of

Cardiology and the North American Society of Pacing and

Electrophysiology, 1996;Berntson et al., 1997) inﬂuenced how

researchers reported and interpreted HRV. The guidelines

proposed an extraction of high and low frequency bands from

the heart rate spectrum. The high frequency band (HF) was

assumed to represent vagal inﬂuences and to be statistically

equivalent to the time domain methods frequently used to

calculate RSA. The low frequency band (LF) has been

considered to be either a marker of sympathetic modulation

(e.g., Malliani et al., 1991) or inﬂuenced by both sympathetic

and vagal inﬂuences (Akselrod et al., 1981). Researchers also

proposed a ratio measure as a potential index of sympathico-

vagal balance (Pagani et al., 1986). Many investigators assume

that the frequency bands deﬁne variables that accurately assess

vagal and sympathetic inﬂuences.

There are inherent problems with selecting frequency bands

to quantify HRV without an understanding of neurophysiolo-

gical mechanisms. These problems are exacerbated when the

techniques are applied independent of an understanding that

respiration parameters are age, species, and context dependent.

In several experimental contexts, individual differences in

spontaneous breathing rate are distributed across a broad range

of frequencies, with individuals with faster breathing frequen-

cies contributing to the HF band and individuals with slower

breathing frequencies contributing to the LF band. Also

problematic are manipulations that are assumed to control for

variations in breathing, such as slow paced breathing (i.e.,

outside the frequencies deﬁning HF), which would be

represented not in the HF band, but in the LF band. In both

cases, HF would no longer accurately describe RSA. However,

it is possible to use a frequency band in the heart rate spectrum

to quantify RSA, when the distribution of breathing frequencies

is spontaneous and conﬁrmed to reside within a selected

spectral band. As demonstrated in the Denver et al. (this

volume) study, the spectral decomposition of HRV provides a

reliable method to estimate breathing frequency and to conﬁrm

(even if respiration is not monitored) that the selection of the

frequency band to represent RSA is inclusive of individual

differences in spontaneous breathing frequencies.

A disconnect between operationally deﬁned objective

measures and the physiological processes that mediate these

measures has resulted in inappropriate analysis strategies.

Studies have reported correlations between HF and RSA, as if

these were different processes. In addition, researchers have

used the frequency parameters for HF and LF developed for

adult studies on human neonates (who breathe substantially

faster than adults), without a consideration of what the

frequency bands reﬂect in terms of neurophysiological

processes.

The quantiﬁcation of RSA is an important step towards the

treatment of HRV as a deﬁned physiological process with a

speciﬁc identiﬁable neurophysiological mechanism. Tradi-

tional physiological techniques (i.e., cholinergic blockade with

atropine) determined that RSA, as a physiological variable, is a

vagal phenomenon. In our laboratory, we have focused on

developing methods designed to extract accurate measures of

RSA. Our methods modiﬁed time-series technologies to

conform to the dynamic and often non-stationary character-

istics of the beat-to-beat heart rate pattern (Porges and Bohrer,

1990; Porges and Byrne, 1992). These methods assume that

HRV is a complex process in which components dynamically

vary. Our methods provided new opportunities to measure how

RSA interacts with behavior, psychological processes, and

neurophysiological mechanisms. The methods, however, made

no explicit assumption regarding potential inﬂuences on RSA

from other variables, including pulmonary, movement, and the

inﬂuence of special visceral efferent pathways such as nerves

regulating laryngeal activity that also originate in the nucleus

ambiguus. Rather, the availability of these methods provides an

opportunity to evaluate and to study the dynamics of possible

covariation and interaction between RSA and other physiolo-

gical variables. From the polyvagal perspective, RSA is a direct

measure of the vagal efferent outﬂow originating in the nucleus

ambiguus that inﬂuences the nicotinic preganglionic receptors

on the sino-atrial node. Thus, the measurement of RSA

provides a unique opportunity for psychophysiologists to

monitor central regulation via a peripheral measure of a neural

circuit involved in the coordination of visceral state and the

expression of emotion and social communication.

Consistent with the polyvagal perspective, our interest in

RSA focuses on the established ﬁndings that the cardioinhi-

bitory vagal ﬁbers that originate in the nucleus ambiguus have a

respiratory rhythm. To emphasize that our measure of RSA

reﬂected vagal inﬂuences only from the nucleus ambiguus, we

labeled the variable, V

(Porges et al., 1996). The amplitude of

RSA, which we, as well as others (e.g., Grossman and Svebak,

1987), had assumed to be an index of cardiac vagal tone, was

S.W. Porges / Biological Psychology 74 (2007) 116–143 135

redeﬁned to emphasize that RSA represented only the

functional output of the vagal efferent pathways originating

from the nucleus ambiguus that terminate on the sino-atrial

node. In the past, we have not deﬁned or speculated what would

index vagal efferent pathways originating in the dorsal motor

nucleus of the vagus. However, in this paper, a method will be

proposed to separate and quantify the two vagal sources from

the beat-to-beat heart rate pattern.

4.8. Respiration and RSA

From a physiological perspective, RSA has been assumed to

be related to breathing. For example, studies were conducted to

evaluate the effect of breathing frequency and tidal volume on

RSA (Hirsch and Bishop, 1981; Eckberg, 2003). These studies

were conducted through the ‘‘lens’’ of a peripheral physio-

logical model in which RSA was construed to be a dependent

variable. Insights from contemporary neurophysiology and

neuroanatomy have changed our view of how respiration and

RSA are related. First, the medullary region, in which the vagal

ﬁbers producing RSA originate, are inherently silent and

require input from other neural pathways in the brain to

activate and produce the output that is manifested as RSA.

Second, common medullary structures are involved in the

regulation of both respiration and RSA. Third, afferent

feedback, not only from the pulmonary stretch receptors,

but also from chemoreceptors, baroreceptors, and other

afferents traveling through the afferent vagus, inﬂuence the

central mechanisms mediating RSA. Fourth, neuropeptides

such as oxytocin and vasopressin inﬂuence the medullary

structures regulating RSA (see Porges, 2003). Finally, higher

brain structures modulate the output of the medullary nuclei

and dynamically adjust the ‘‘gain’’ of the afferent feedback on

the medullary structures regulating RSA.

It has been argued that RSA cannot be measured without

‘‘pacing’’ breathing or statistically correcting for respiration.

What is the basis for these arguments? What does the literature

tell us? A survey of the literature (see Denver et al., this issue)

argues that during spontaneous breathing baselines, breathing

frequency is not related to RSA. Even inspection of the early

studies manipulating breathing illustrate that the strongest

effect on RSA occurs when breathing is paced substantially

slower than the spontaneous rate (Hirsch and Bishop, 1981).

However, during conditions requiring an increase in cardiac

output, within subject correlations illustrate a coordinated

linear relation between breathing frequency and a decrease in

RSA (e.g., Hatﬁeld et al., 1998). Although tidal volume is

inﬂuenced by changes in cardiac activity, the relationship with

RSA is not linear (e.g., Hatﬁeld et al., 1998).

If the relation between spontaneous breathing frequency and

RSA is weak and may vary from study to study (and perhaps

from condition to condition within subject), why is this a major

argument? If the relation between RSA and tidal volume is not

linear, why would linear regression models be used (e.g.,

Grossman et al., 2004)? Is this bias due to the method of RSA

quantiﬁcation? The strongest proponents for ventilatory

corrections employ peak–trough methods, a technique that

has been demonstrated to be vulnerable to breathing frequency

(see Byrne and Porges, 1993).

Although methodology might contribute to the debate, it is

not the prime issue in understanding the justiﬁcation for

advocating correction procedures for RSA. Rather, the debate

focuses on the conﬂict between fundamentally different levels

of inquiry and how these different levels foster the statement of

research questions. The physiological perspective asks research

questions relating RSA to cardiac vagal tone. The polyvagal

perspective asks research questions relating RSA to neural

circuits and linking these circuits to cognitive, affective, and

health processes. The physiological perspective focuses on

physiological models in which cardiac vagal tone is an accepted

and meaningful construct when describing autonomic regula-

tion. The polyvagal perspective focuses on the neuroanatomi-

cal, neurophysiological, and functional differences between the

two vagal pathways. For example, from a physiological level of

inquiry, research may be focused on establishing RSA as an

index of cardiac vagal tone by applying regression models to

improve the covariation of RSA with change in heart rate in

response to atropine. This research strategy might include

statistical adjustments involving measures of pulmonary

function and motor activity. In contrast, from a polyvagal

perspective, research is directed at investigations of the speciﬁc

vagal pathways that originate in the two source nuclei, the

nucleus ambiguus and the dorsal motor nucleus. From the

polyvagal perspective, statistical adjustments (e.g., regression

models adjusting for pulmonary variables) or pacing of

breathing confound and distort RSA as a measure of the direct

neural outﬂow from the nucleus ambiguus. This does not

preclude the study of a global cardiac vagal tone that would

include the sum of the efferent outﬂow from the source nuclei of

both vagal pathways. For example, concepts of autonomic

balance might be better described on the physiological level,

since the focus is on the state of the peripheral organ.

Arguing that RSA correction procedures are a methodolo-

gical issue has displaced the important dialogue questioning

fundamental levels of inquiry and their related paradigms.

Thus, the focus on methods and the proposition that RSA

cannot be quantiﬁed without correcting or adjusting for

respiration silenced the opportunity to question the mechanisms

mediating RSA, the criteria for measures of cardiac vagal tone,

and the use of measures of cardiac vagal tone in psychophy-

siological research.

4.9. Is RSA a valid measure of cardiac vagal tone?

This question depends on how cardiac vagal tone is

operationally deﬁned. The literature reliably demonstrates that

cholinergic blockade depresses RSA, while RSA is insensitive to

B-adrenergic blockade. Thus, the argument is not whether RSA

is mediated via vagal pathways, but whether RSA can be a

surrogate measure of cardiac vagal tone. Following a physio-

logical perspective, changes in heart rate in response to

cholinergic blockade has served as a surrogate criterion variable

for cardiac vagal tone. This surrogate variable can be correlated

with either RSA or change in RSA to the blockade. When these

S.W. Porges / Biological Psychology 74 (2007) 116–143136

variables are correlated, the relations are very strong, but not

perfect. From a physiological perspective, this points to a

weakness in RSA as an index of cardiac vagal tone and leads to

strategies to ‘‘correct’’ RSA. However, from a neurophysiolo-

gical perspective, this discrepancy is obvious. First, RSA is vagal,

but it reﬂects only the vagal efferent pathways from the nucleus

ambiguus. The vagal inﬂuence from the dorsal motor nucleus of

the vagus is not included in the calculation of RSA, although it

contributes to heart rate.

Why should corrections related to respiration improve the

sensitivity of RSA to cardiac vagal tone? Cardiac vagal tone, by

deﬁnition, represents inﬂuences from both vagal nuclei to the

sino-atrial node. This can be described by the following

heuristic model: CVT = NA + DMX (CVT is cardiac vagal

tone, NA is the vagal tone originating from the nucleus

ambiguus, DMX is the vagal tone originating from the dorsal

motor nucleus of the vagus). In this model, RSA can be

substituted for NA (CVT = RSA + DMX). Thus, if atropine

blockade affects the post-ganglionic transmission from both

vagal pathways, the relation between changes in cardiac vagal

tone and changes in RSA should be monotonic, but not unity.

This, of course, is seen in Fig. 3 from the atropine dose response

study.

Based on data obtained using the physiologist’s toolbox, a

strong argument could be made that RSA is a ﬁne surrogate for

cardiac vagal tone. However, this proposition is based on an

assumption that the vagal inﬂuences originating in the dorsal

motor nucleus of the vagus are constant or minimal. Without

measuring this vagal component, the covariation between

cardiac vagal tone and RSA would be dependent of the state of

the dorsal vagal system. The polyvagal theory has provided a

perspective to study states in which the two systems deviate.

For example, there are easily identiﬁed clinical conditions of

severe and potentially lethal bradycardia that are mediated by

the vagus in the absence of RSA (see Reed et al., 1999).

Is the output of the dorsal motor nucleus of the vagus

inﬂuencing heart rate and the surrogate measures of cardiac

vagal tone? Applying the polyvagal perspective to this question

provides both an explanation of ‘‘why’’ paced breathing might

improve the covariation with traditional global measures of

cardiac vagal tone, and how to devise a method to extract a

dynamic index of the changing inﬂuence of the DMX on the

heart.

In a bold paper, Eckberg (1997) challenged the use of the LF

component as an index of sympathico-vagal tone balance. The

paper resulted in an interesting dialogue published in

conjunction with Eckberg’s article in Circulation. Eckberg

described the paradox in which LF was sensitive to atropine,

although argued to be a sensitive indicator of sympathetic

activity. Most interesting, this point was not refuted in any of

the comments following the paper. We observed the same

effect. As illustrated in Fig. 3, LF follows an atropine dose–

response curve similar to both RSA and heart period. Note that

the effect sizes for LF were equivalent with RSA and about

twice the size as heart period, thus, demonstrating the

dependence of the LF (i.e., THM) on vagal pathways (see

Fig. 4). In other research, we demonstrated that this frequency

band was selectively sensitive to vagal blockade and that

sympathetic blockade had no effect. Other researchers have

argued similar points (Houle and Billman, 1999).

If the LF is not a direct index of sympathetic inﬂuences on

the heart, could it reﬂect activity from the DMX? Knowledge

regarding the inﬂuence of vagal ﬁbers on the heart rate pattern

is expanding. In 1995, when the polyvagal theory was

published, little was known about the impact on the heart

via the C-ﬁbers originating in the DMX. It was assumed that the

primary vagal inﬂuence on the heart was mediated via the B-

ﬁbers originating in the nucleus ambiguus. In addition, since

few DMX ﬁbers synapse on the sino-atrial node, it was thought

that their impact on the regulation of heart rate would be

minimal. Unlike global measures of heart rate or HRV, RSAwas

solely regulated via vagal ﬁbers originating in the nucleus

ambiguus. Thus, it appeared that RSA would be an excellent

criterion variable for cardiac vagal tone. However, recent

ﬁndings in neuroanatomy and neurophysiology force a

reconceptualization of cardiac vagal tone and measures of

HRV. This new conceptualization provides us with a basis to

propose that the spectral decomposition of HRV may provide

information regarding the function of both NA and DMX vagal

pathways.

There is little disagreement regarding the robust relation

between RSA and vagal efferent activity being transmitted

from the nucleus ambiguus through the myelinated vagal ﬁbers

to the heart. The rapid transmission through nicotinic pregan-

glionic receptors provides an opportunity to track this system,

even when respiratory frequencies are very high. Contempor-

ary research on the DMX pathways suggests that, due to

unmyelinated ﬁbers and preganglionic muscarinic receptors,

cardioinhibitory trafﬁc is slower than that originating in the

nucleus ambiguus (Cheng and Powley, 2000). There are

several important unanswered questions about the mechanisms

and the function of these pathways on the heart. These issues

include questions related to the number of preganglionic and

post-ganglionic ﬁbers, the ratio of preganglionic to post-

ganglionic ﬁbers, and the speciﬁc cardiac function of these

pathways.

If we assume that CVT = LF + RSA, we can approach this

model through a physiological level of inquiry. First, we could

block the effect of the nicotinic receptors with hexamethonium

and evaluate the effect on HRV. Since hexamethonium

selectively blocks nicotinic acetylcholine receptors, it would

blockthevagaltrafﬁcoriginatingonlyinthenucleus

ambiguus. The literature demonstrates selective blockade of

these pathways in animal models (e.g., Cheng and Powley,

2000), but has not evaluated its effect on RSA and whether

slower oscillations remain in the heart rate spectrum. Research

needs to be directed to evaluate changes in the heart rate

spectrum in animal models following the administration of

hexamethonium. Interestingly, since several inhalant anes-

thetics block nicotinic receptors, validation of the sensitivity of

RSA to the nicotinic pathways could be demonstrated by

monitoring RSA during the induction and maintenance of

anesthesia. Under these conditions, RSA could potentially be a

useful selective marker of depth of anesthesia. In the ﬁrst

S.W. Porges / Biological Psychology 74 (2007) 116–143 137

demonstration that the quantiﬁcation of RSA could be used as

an index of depth of inhalant anesthesia, we reported that

isoﬂurane selectively depressed RSA, while not reliably

inﬂuencing heart period (Donchin et al., 1985). At the time of

the study, the mechanism through which isoﬂurane inﬂuenced

RSA was not known. Consistent with the polyvagal perspec-

tive, a ﬁgure in the paper documents that the slower oscillations

(LF) in the beat-to-beat pattern were preserved during

anesthesia, while RSA was totally depressed. Thus, the

depression of RSA might be due to the selective impact of

isoﬂurane on the preganglionic nicotinic receptors that

characterize the myelinated vagal pathways originating in

the nucleus ambiguus.

Alternatively, paced breathing could be used to shift the

frequency of RSA towards the endogenous rhythm associated

with LF. Under conditions when participants pace breathing at

0.1 Hz, the LF (0.06–0.1 Hz) would include RSA. During this

unique manipulation, if we assume that DMX pathways

contribute to LF during spontaneous breathing, then slow paced

breathing in the LF band would represent the summed inﬂuence

of both DMX and NA vagal pathways on the heart.

Interestingly, this may be the neurophysiological substrate

underlying how manipulation of ventilatory parameters can

change the covariation between RSA and surrogate measures of

total cardiac vagal tone. However, under these constrained

conditions, it would be impossible to extract information

regarding the function of the two vagal systems. Also, we need

to question whether a global measure of cardiac vagal tone is of

use to psychophysiologists. Other strategies, relying on

statistical adjustments based on simultaneously monitored

ventilatory parameters, often result in derived variables

adjusting RSA, not only by breathing frequency, but also by

tidal volume (e.g., Grossman et al., 2004). If these derived

variables are to be used as a surrogate measure for global

cardiac vagal tone, generalizability needs to be investigated to

determine whether they reﬂect parameters of an over speciﬁed

statistical model.

The polyvagal perspective approaches questions regarding

mechanisms, adaptive function, and speciﬁc neural pathways.

In dealing with investigations relating respiration to RSA, the

strategy focuses on central neural regulation and does not focus

on peripheral physiology. The polyvagal perspective directs,

based on our current interests, research questions towards the

involvement of the nucleus ambiguus in regulating heart rate

(i.e., producing RSA) and whether this area of the brainstem is

causal, interactive, or consequential to respiratory and

pulmonary inﬂuences. From this perspective, several research

questions would be of interest. Since afferents from the

trigeminal and facial nerves provide input to the nucleus

ambiguus, the polyvagal perspective would focus on the

inﬂuence of respiratory resistance on RSA (e.g., Sargunaraj

et al., 1996).

The concept of a common cardiopulmonary oscillator ﬁts

well within a polyvagal perspective. Researchers have

documented the importance of a hypothetical ‘‘respiratory

gate’’ on the vagal outﬂow (see Eckberg, 2003). Since the

respiratory rhythm is selectively gating only the vagal outﬂow

from the nucleus ambiguus, the polyvagal theory would

speculate that inspiration/expiration (I/E) ratios would inﬂu-

ence the amplitude of RSA. Based on this neurophysiological

model, vagal outﬂow to the sino-atrial node increases during

expiration, with higher amplitude of RSA being associated with

relatively longer exhalation durations. Thus, the amplitude of

RSA should be related to the ratio of inspiratory and expiratory

durations. There are two ways of approaching this hypothesis:

(1) manipulating inspiration and expiration ratios during paced

breathing, or (2) evaluating individual differences during

spontaneous baseline breathing. The ﬁrst strategy may

confound the phenomenon, since task demands and the

deviation from normal breathing patterns might trigger

adaptive changes in autonomic state. The second strategy

may also confound the phenomenon, since during baseline

there is a restricted range of breathing patterns and the I/Eratio

may covary with other variables such as weight, age, and

health.

Strauss-Blache et al. (2000) approached this relation by

manipulating breathing, and in our laboratory we approached the

relation by investigating individual differences during sponta-

neous baseline breathing. Strauss-Blache et al. demonstrated

that, during trials with short inspiration followed by long

expiration, the amplitude of RSA was signiﬁcantly greater than

during trials with long inspiration followed by short expiration.

These effects could not be accounted for by differences in

breathing rate or amplitude. In our laboratory, we conducted a

naturally occurring experiment relating individual differences in

the I/Eratio to RSA. We monitored participants during a baseline

condition with a Vivometrics LifeShirt. The LifeShirt monitors

ECG and several ventilatory parameters including calibrated

measures of tidal volume, inspiration and expiration duration,

and breathing rate. Consistent with the Strauss-Blache et al.

study, we observed that the I/Eratio was signiﬁcantly related to

the amplitude of RSA (r(41) = .50, p<.001). However, the

relations between RSA and both respiration frequency (r=.08)

and tidal volume (r=.11) were not signiﬁcant.

4.10. Conclusion

The polyvagal perspective is an attempt to apply constructs

derived from the polyvagal theory to understand the

discrepancies in the literature related to method of measure-

ment, neurophysiological and neuroanatomical mechanisms,

and adaptive functions of vagal efferent pathways. The

approach emphasizes that biases or discipline myths occur

when investigations are limited to psychological or physiolo-

gical levels of inquiry. The polyvagal perspective proposes that

it is necessary, not only to understand the vagal efferent actions

on the heart from a neurophysiological level of inquiry, but also

the adaptive function of neural regulation of the heart,

interpreted within the context of the phylogeny of the

autonomic nervous system. In the sections above, several

discipline myths have been deconstructed and interpreted based

on level of inquiry. These points are summarized below to

provide targeted statements to stimulate further scientiﬁc

investigations and challenges via well-designed experiments.

S.W. Porges / Biological Psychology 74 (2007) 116–143138

4.10.1. Discipline myth 1: cardiac vagal tone is a useful

construct in psychophysiological research

Although tonic measures of cardiac vagal tone have an

important role in understanding visceral states and in

developing constructs related to autonomic balance, it is of

limited use in describing and understanding response strategies

to environmental and visceral stimuli. Cardiac vagal tone as a

global construct provides limited information regarding

speciﬁcity of the neural mechanisms through which heart rate

patterns react to speciﬁc psychological stimuli, reﬂect health

risk, and change with interventions or challenges. Measures of

more speciﬁc vagal regulation, via either the nucleus ambiguus

(i.e., RSA) or the dorsal motor nucleus (i.e., LF), may provide

more meaningful information.

4.10.2. Discipline myth 2: to be a meaningful index of

vagal inﬂuences, RSA must be adjusted by either paced

breathing or by statistically adjusting for ventilatory

parameters

The motivation to adjust RSA is based on empirical reports

of a divergence between surrogate measures of cardiac vagal

tone and RSA. Adjustments are proposed to improve the

relation between RSA and the surrogate measure for total

cardiac vagal tone. Although RSA is not the equivalent of total

cardiac vagal tone, as an ‘‘index’’ of total cardiac vagal tone, it

is at least as sensitive to blockade as traditional measures.

Moreover, the validity of ‘‘adjusted’’ RSA variables as indices

of cardiac vagal tone needs to be challenged by conducting

dose–response blockade challenges. Even if RSA were not as

sensitive as other indices of total cardiac vagal tone, RSA

should be studied without adjustment. RSA is an important

variable reﬂecting the functional output of speciﬁc vagal

pathways originating in the nucleus ambiguus that are

neurophysiologically and neuroanatomically linked to several

processes of interest to psychophysiologists (e.g., emotion,

social engagement, ingestion, health). Thus, there is no

advantage in correcting RSA to map into a global surrogate

variable for total cardiac vagal tone.

4.10.3. Discipline myth 3: the low frequency (LF) in the

heart rate spectrum is related to sympathetic activity or

sympathetic-vagal balance

The low frequency in the heart rate spectrum is exquisitely

sensitive to muscarinic blockade. LF can be totally blocked when

the vagal efferent inﬂuences are blocked. In fact, LF is as

sensitive to vagal blockade as RSA and more sensitive to vagal

blockade than heart rate. Although sympathetic inﬂuences might

be involved in triggering this neural circuit, the ﬁnal common

pathway is purely vagal. Since features of this periodicity

respond differently than RSA to various challenges and appear to

be preserved during inhalant anesthesia, the time course of LF

may index vagal output from the dorsal motor nucleus.

4.10.4. Discipline myth 4: methods to quantify RSA are

equivalent, if they are highly correlated

High correlations, even those above 0.9, can be demon-

strated between low and high-resolution measures. Measures

that smooth across a broad range of individual and intra-

individual differences may be correlated with methods that

provide high resolution and greater sensitivity to experimental

manipulations or diagnostic features. Measures that have poor

precision in timing, poor accuracy in detecting the peak of the

R-wave, and may be inﬂuenced by other sources of variance

including baseline trends, may be highly correlated with more

precise and accurate measures of RSA that incorporate

statistically well deﬁned algorithms to extract accurately the

amplitude of RSA. These high correlations are not arguments

for equivalence. More appropriate tests would contrast size of

effects in response to known methods of vagal blockade,

including manipulations that would selectively block or

increase the outﬂow from the source nuclei of the myelinated

vagal efferents located in nucleus ambiguus.

The polyvagal perspective, with an emphasis on nervous

system regulation, is a major shift for psychophysiological

researchers, who historically have not attributed mechanism to

heart rate or HRV. In addition, this perspective leads the

researcher to ask new questions, including such rudimentary

issues as the establishment of data collection parameters, the

methods developed to quantify various components of the heart

rate pattern, and even the strategies used to correct artifact. The

polyvagal perspective encourages researchers interested in

autonomic-behavioral relations to expand their research agenda

to include questions related to: (1) features of the source nuclei

in the nucleus ambiguus and the dorsal motor nucleus of the

vagus, (2) inﬂuences of the afferent vagus via the nucleus

tractus solitarius on the source nuclei of both vagi, (3) the

inﬂuence of ascending pathways from the nucleus tractus

solitarius on brain areas regulating cognition and affect, (4) the

functional differences between the vagal efferent pathways

characterized by preganglionic nicotinic and muscarinic

acetylcholine receptors, (5) the functional differences in the

effect of myelinated and unmyelinated vagal efferent pathways

on the sino-atrial node, (6) the interaction between the

regulation of the special visceral efferent and myelinated

vagal pathways, and (7) the inﬂuence of peripheral and central

structures and circuits on modulating the output of the vagal

efferent pathways.

By investigating the contradiction between methods used to

measure RSA, we can see how different research questions and

assumptions lead to different methods and paradigms. When

research strategies are based on a peripheral physiological level

of inquiry, then cardiac vagal tone is assumed to represent a

unitary construct. However, when research strategies are based

on a neurophysiological level of inquiry, then the quest for a

measure of cardiac vagal tone is reﬁned to focus on methods that

selectively measure each of the two vagal systems. The latter

strategy should be appealing to psychophysiologists, since the

two vagal systems evolved to support different classes of

behavior. Vagal activity originating in the nucleus ambiguus is

neurophysiologically and neuroanatomically linked to the

regulation of the striated muscles of the face and head, structures

that are involved in social interaction and emotion. Theoretically,

RSA should closely parallel individual and intra-individual

variations in emotion expression, social communication, and

S.W. Porges / Biological Psychology 74 (2007) 116–143 139

behavioral state. In contrast, vagal activity originating in the

DMX should reﬂect tonic inﬂuences to the visceral organs (i.e.,

primarily subdiaphragmatic). Rapid and massive increases in the

output of the DMX that may produce bradycardia, apnea, or

defecation would occur as a defense strategy to reduce metabolic

demands. Perhaps, the negative features of stress and health

vulnerability being associated with the slower rhythms may have

led scientists to assume that these rhythms were inﬂuenced by the

sympathetic nervous system.

The polyvagal perspective shifts research from atheoretical

strategies towards theory driven paradigms dependent upon

explicit neural mechanisms. Foremost, the polyvagal perspec-

tive emphasizes the importance of phylogenetic changes in the

neural structures regulating the autonomic nervous system. The

phylogenetic strategy provides insights into the adaptive

function and the neural regulation of the two vagal systems

(see Porges, 1995, 2001a). Without having constructs from the

polyvagal theory to describe adaptive functions and to

determine the measurement speciﬁcations of the two vagal

systems (one associated with calm states and social engagement

behaviors and the other a vestigial defense system that is

potentially lethal to mammals), it would not be possible to

disentangle the mechanisms and functions of the components of

cardiac vagal tone.

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